Merge tag 'v5.3.0' of github.com:prysmaticlabs/prysm

Fix Blobs By Range RPC Handler (#14910 )
* Add tests for TestSendBlobsByRangeRequest. Currently not working with sequential blob validation. * Copy Root First * Allow Test For Maximum Amount of Blobs * Fails with the Same error * Fix Last Test Assertion * Add in Fix * Changelog --------- Co-authored-by: Preston Van Loon <preston@pvl.dev>
2026-01-10 05:47:59 -05:00 · 2025-02-12 12:59:53 -06:00 · 2025-02-11 14:11:12 +00:00 · 2025-02-11 13:44:00 +00:00 · 2025-02-10 23:50:09 +00:00 · 2025-02-10 15:12:57 +00:00
341 changed files with 14994 additions and 10742 deletions
--- a/.bazelversion
+++ b/.bazelversion
@@ -1 +1 @@
-7.1.0
+7.4.1
--- a/.github/actions/gomodtidy/Dockerfile
+++ b/.github/actions/gomodtidy/Dockerfile
@@ -1,4 +1,4 @@
-FROM golang:1.22-alpine
+FROM golang:1.23-alpine

 COPY entrypoint.sh /entrypoint.sh

--- a/.github/workflows/clang-format.yml
+++ b/.github/workflows/clang-format.yml
@@ -0,0 +1,21 @@
+name: Protobuf Format
+
+on: 
+  push:
+    branches: [ '*' ]
+  pull_request:
+    branches: [ '*' ]
+  merge_group:
+    types: [checks_requested]
+
+jobs:
+  clang-format-checking:
+    runs-on: ubuntu-latest
+    steps:
+      - uses: actions/checkout@v2
+      # Is this step failing for you? 
+      # Run: clang-format -i proto/**/*.proto
+      # See: https://clang.llvm.org/docs/ClangFormat.html
+      - uses: RafikFarhad/clang-format-github-action@v3
+        with:
+          sources: "proto/**/*.proto"
--- a/.github/workflows/fuzz.yml
+++ b/.github/workflows/fuzz.yml
@@ -16,7 +16,7 @@ jobs:
      - uses: actions/checkout@v3
      - uses: actions/setup-go@v4
        with:
-          go-version: '1.22.10'
+          go-version: '1.23.5'
      - id: list
        uses: shogo82148/actions-go-fuzz/list@v0
        with:
@@ -36,7 +36,7 @@ jobs:
      - uses: actions/checkout@v3
      - uses: actions/setup-go@v4
        with:
-          go-version: '1.22.10'
+          go-version: '1.23.5'
      - uses: shogo82148/actions-go-fuzz/run@v0
        with:
          packages: ${{ matrix.package }}
--- a/.github/workflows/go.yml
+++ b/.github/workflows/go.yml
@@ -28,10 +28,10 @@ jobs:
    steps:
      - name: Checkout
        uses: actions/checkout@v4
-      - name: Set up Go 1.22
+      - name: Set up Go 1.23
        uses: actions/setup-go@v4
        with:
-          go-version: '1.22.10'
+          go-version: '1.23.5'
      - name: Run Gosec Security Scanner
        run: | # https://github.com/securego/gosec/issues/469
          export PATH=$PATH:$(go env GOPATH)/bin
@@ -45,16 +45,16 @@ jobs:
      - name: Checkout
        uses: actions/checkout@v4

-      - name: Set up Go 1.22
+      - name: Set up Go 1.23
        uses: actions/setup-go@v4
        with:
-          go-version: '1.22.10'
+          go-version: '1.23.5'
          id: go

      - name: Golangci-lint
        uses: golangci/golangci-lint-action@v5
        with:
-          version: v1.56.1
+          version: v1.63.4
          args: --config=.golangci.yml --out-${NO_FUTURE}format colored-line-number

  build:
@@ -64,7 +64,7 @@ jobs:
      - name: Set up Go 1.x
        uses: actions/setup-go@v4
        with:
-          go-version: '1.22.10'
+          go-version: '1.23.5'
        id: go

      - name: Check out code into the Go module directory
--- a/.golangci.yml
+++ b/.golangci.yml
@@ -1,28 +1,20 @@
 run:
-  skip-files:
+  timeout: 10m
+  go: '1.23.5'
+
+issues:
+  exclude-files:
    - validator/web/site_data.go
    - .*_test.go
-  skip-dirs:
+  exclude-dirs:
    - proto
    - tools/analyzers
-  timeout: 10m
-  go: '1.22.10'

 linters:
  enable-all: true
  disable:
    # Deprecated linters:
-    - deadcode
-    - exhaustivestruct
-    - golint
    - govet
-    - ifshort
-    - interfacer
-    - maligned
-    - nosnakecase
-    - scopelint
-    - structcheck
-    - varcheck

    # Disabled for now:
    - asasalint
@@ -34,6 +26,8 @@ linters:
    - dogsled
    - dupl
    - durationcheck
+    - errname
+    - err113
    - exhaustive
    - exhaustruct
    - forbidigo
@@ -47,17 +41,17 @@ linters:
    - gocyclo
    - godot
    - godox
-    - goerr113
    - gofumpt
-    - gomnd
    - gomoddirectives
    - gosec
    - inamedparam
    - interfacebloat
+    - intrange
    - ireturn
    - lll
    - maintidx
    - makezero
+    - mnd
    - musttag
    - nakedret
    - nestif
@@ -72,6 +66,7 @@ linters:
    - predeclared
    - promlinter
    - protogetter
+    - recvcheck
    - revive
    - spancheck
    - staticcheck
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -60,7 +60,7 @@ Notable features:
 - Updated the default `scrape-interval` in `Client-stats` to 2 minutes to accommodate Beaconcha.in API rate limits.
 - Switch to compounding when consolidating with source==target.
 - Revert block db save when saving state fails.
- Return false from HasBlock if the block is being synced. 
+- Return false from HasBlock if the block is being synced.
 - Cleanup forkchoice on failed insertions.
 - Use read only validator for core processing to avoid unnecessary copying.
 - Use ROBlock across block processing pipeline.
@@ -73,7 +73,7 @@ Notable features:
 - Simplified `EjectedValidatorIndices`.
 - `engine_newPayloadV4`,`engine_getPayloadV4` are changes due to new execution request serialization decisions, [PR](https://github.com/prysmaticlabs/prysm/pull/14580)
 - Fixed various small things in state-native code.
- Use ROBlock earlier in block syncing pipeline. 
+- Use ROBlock earlier in block syncing pipeline.
 - Changed the signature of `ProcessPayload`.
 - Only Build the Protobuf state once during serialization.
 - Capella blocks are execution.
@@ -139,9 +139,9 @@ Notable features:

 ### Security

-## [v5.1.2](https://github.com/prysmaticlabs/prysm/compare/v5.1.1...v5.1.2) - 2024-10-16 
+## [v5.1.2](https://github.com/prysmaticlabs/prysm/compare/v5.1.1...v5.1.2) - 2024-10-16

-This is a hotfix release with one change. 
+This is a hotfix release with one change.

 Prysm v5.1.1 contains an updated implementation of the beacon api streaming events endpoint. This
 new implementation contains a bug that can cause a panic in certain conditions. The issue is
@@ -153,20 +153,20 @@ prysm REST mode validator (a feature which requires the validator to be configur
 api instead of prysm's stock grpc endpoints) or accessory software that connects to the events api,
 like https://github.com/ethpandaops/ethereum-metrics-exporter

-### Fixed 
+### Fixed

 - Recover from panics when writing the event stream [#14545](https://github.com/prysmaticlabs/prysm/pull/14545)

 ## [v5.1.1](https://github.com/prysmaticlabs/prysm/compare/v5.1.0...v5.1.1) - 2024-10-15

-This release has a number of features and improvements. Most notably, the feature flag 
-`--enable-experimental-state` has been flipped to "opt out" via `--disable-experimental-state`. 
+This release has a number of features and improvements. Most notably, the feature flag
+`--enable-experimental-state` has been flipped to "opt out" via `--disable-experimental-state`.
 The experimental state management design has shown significant improvements in memory usage at
 runtime. Updates to libp2p's gossipsub have some bandwidith stability improvements with support for
-IDONTWANT control messages. 
+IDONTWANT control messages.

 The gRPC gateway has been deprecated from Prysm in this release. If you need JSON data, consider the
-standardized beacon-APIs. 
+standardized beacon-APIs.

 Updating to this release is recommended at your convenience.

@@ -208,7 +208,7 @@ Updating to this release is recommended at your convenience.
 - `grpc-gateway-corsdomain` is renamed to http-cors-domain. The old name can still be used as an alias.
 - `api-timeout` is changed from int flag to duration flag, default value updated.
 - Light client support: abstracted out the light client headers with different versions.
- `ApplyToEveryValidator` has been changed to prevent misuse bugs, it takes a closure that takes a `ReadOnlyValidator` and returns a raw pointer to a `Validator`. 
+- `ApplyToEveryValidator` has been changed to prevent misuse bugs, it takes a closure that takes a `ReadOnlyValidator` and returns a raw pointer to a `Validator`.
 - Removed gorilla mux library and replaced it with net/http updates in go 1.22.
 - Clean up `ProposeBlock` for validator client to reduce cognitive scoring and enable further changes.
 - Updated k8s-io/client-go to v0.30.4 and k8s-io/apimachinery to v0.30.4
@@ -219,7 +219,7 @@ Updating to this release is recommended at your convenience.
 - Updated Sepolia bootnodes.
 - Make committee aware packing the default by deprecating `--enable-committee-aware-packing`.
 - Moved `ConvertKzgCommitmentToVersionedHash` to the `primitives` package.
- Updated correlation penalty for EIP-7251. 
+- Updated correlation penalty for EIP-7251.

 ### Deprecated
 - `--disable-grpc-gateway` flag is deprecated due to grpc gateway removal.
@@ -693,34 +693,34 @@ AVX support (eg Celeron) after the Deneb fork. This is not an issue for mainnet.

 - Linter: Wastedassign linter enabled to improve code quality.
 - API Enhancements:
-    - Added payload return in Wei for /eth/v3/validator/blocks.
-    - Added Holesky Deneb Epoch for better epoch management.
+  - Added payload return in Wei for /eth/v3/validator/blocks.
+  - Added Holesky Deneb Epoch for better epoch management.
 - Testing Enhancements:
-    - Clear cache in tests of core helpers to ensure test reliability.
-    - Added Debug State Transition Method for improved debugging.
-    - Backfilling test: Enabled backfill in E2E tests for more comprehensive coverage.
+  - Clear cache in tests of core helpers to ensure test reliability.
+  - Added Debug State Transition Method for improved debugging.
+  - Backfilling test: Enabled backfill in E2E tests for more comprehensive coverage.
 - API Updates: Re-enabled jwt on keymanager API for enhanced security.
 - Logging Improvements: Enhanced block by root log for better traceability.
 - Validator Client Improvements:
-    - Added Spans to Core Validator Methods for enhanced monitoring.
-    - Improved readability in validator client code for better maintenance (various commits).
+  - Added Spans to Core Validator Methods for enhanced monitoring.
+  - Improved readability in validator client code for better maintenance (various commits).

 ### Changed

 - Optimizations and Refinements:
-    - Lowered resource usage in certain processes for efficiency.
-    - Moved blob rpc validation closer to peer read for optimized processing.
-    - Cleaned up validate beacon block code for clarity and efficiency.
-    - Updated Sepolia Deneb fork epoch for alignment with network changes.
-    - Changed blob latency metrics to milliseconds for more precise measurement.
-    - Altered getLegacyDatabaseLocation message for better clarity.
-    - Improved wait for activation method for enhanced performance.
-    - Capitalized Aggregated Unaggregated Attestations Log for consistency.
-    - Modified HistoricalRoots usage for accuracy.
-    - Adjusted checking of attribute emptiness for efficiency.
+  - Lowered resource usage in certain processes for efficiency.
+  - Moved blob rpc validation closer to peer read for optimized processing.
+  - Cleaned up validate beacon block code for clarity and efficiency.
+  - Updated Sepolia Deneb fork epoch for alignment with network changes.
+  - Changed blob latency metrics to milliseconds for more precise measurement.
+  - Altered getLegacyDatabaseLocation message for better clarity.
+  - Improved wait for activation method for enhanced performance.
+  - Capitalized Aggregated Unaggregated Attestations Log for consistency.
+  - Modified HistoricalRoots usage for accuracy.
+  - Adjusted checking of attribute emptiness for efficiency.
 - Database Management:
-    - Moved --db-backup-output-dir as a deprecated flag for database management simplification.
-    - Added the Ability to Defragment the Beacon State for improved database performance.
+  - Moved --db-backup-output-dir as a deprecated flag for database management simplification.
+  - Added the Ability to Defragment the Beacon State for improved database performance.
 - Dependency Update: Bumped quic-go version from 0.39.3 to 0.39.4 for up-to-date dependencies.

 ### Removed
@@ -731,12 +731,12 @@ AVX support (eg Celeron) after the Deneb fork. This is not an issue for mainnet.
 ### Fixed

 - Bug Fixes:
-    - Fixed off by one error for improved accuracy.
-    - Resolved small typo in error messages for clarity.
-    - Addressed minor issue in blsToExecChange validator for better validation.
-    - Corrected blobsidecar json tag for commitment inclusion proof.
-    - Fixed ssz post-requests content type check.
-    - Resolved issue with port logging in bootnode.
+  - Fixed off by one error for improved accuracy.
+  - Resolved small typo in error messages for clarity.
+  - Addressed minor issue in blsToExecChange validator for better validation.
+  - Corrected blobsidecar json tag for commitment inclusion proof.
+  - Fixed ssz post-requests content type check.
+  - Resolved issue with port logging in bootnode.
 - Test Fixes: Re-enabled Slasher E2E Test for more comprehensive testing.

 ### Security
@@ -1163,9 +1163,9 @@ No security issues in this release.
  now features runtime detection, automatically enabling optimized code paths if your CPU supports it.
 - **Multiarch Containers Preview Available**: multiarch (:wave: arm64 support :wave:) containers will be offered for
  preview at the following locations:
-    - Beacon Chain: [gcr.io/prylabs-dev/prysm/beacon-chain:v4.1.0](gcr.io/prylabs-dev/prysm/beacon-chain:v4.1.0)
-    - Validator: [gcr.io/prylabs-dev/prysm/validator:v4.1.0](gcr.io/prylabs-dev/prysm/validator:v4.1.0)
-    - Please note that in the next cycle, we will exclusively use these containers at the canonical URLs.
+  - Beacon Chain: [gcr.io/prylabs-dev/prysm/beacon-chain:v4.1.0](gcr.io/prylabs-dev/prysm/beacon-chain:v4.1.0)
+  - Validator: [gcr.io/prylabs-dev/prysm/validator:v4.1.0](gcr.io/prylabs-dev/prysm/validator:v4.1.0)
+  - Please note that in the next cycle, we will exclusively use these containers at the canonical URLs.

 ### Added

@@ -2987,4 +2987,4 @@ There are no security updates in this release.

 # Older than v2.0.0

-For changelog history for releases older than v2.0.0, please refer to https://github.com/prysmaticlabs/prysm/releases
+For changelog history for releases older than v2.0.0, please refer to https://github.com/prysmaticlabs/prysm/releases
--- a/MODULE.bazel.lock
+++ b/MODULE.bazel.lock
--- a/46
+++ b/46
@@ -16,6 +16,34 @@ load("@rules_pkg//:deps.bzl", "rules_pkg_dependencies")

 rules_pkg_dependencies()

+load("@bazel_tools//tools/build_defs/repo:http.bzl", "http_archive")
+
+http_archive(
+    name = "toolchains_protoc",
+    sha256 = "abb1540f8a9e045422730670ebb2f25b41fa56ca5a7cf795175a110a0a68f4ad",
+    strip_prefix = "toolchains_protoc-0.3.6",
+    url = "https://github.com/aspect-build/toolchains_protoc/releases/download/v0.3.6/toolchains_protoc-v0.3.6.tar.gz",
+)
+
+load("@toolchains_protoc//protoc:repositories.bzl", "rules_protoc_dependencies")
+
+rules_protoc_dependencies()
+
+load("@rules_proto//proto:repositories.bzl", "rules_proto_dependencies")
+
+rules_proto_dependencies()
+
+load("@bazel_features//:deps.bzl", "bazel_features_deps")
+
+bazel_features_deps()
+
+load("@toolchains_protoc//protoc:toolchain.bzl", "protoc_toolchains")
+
+protoc_toolchains(
+    name = "protoc_toolchains",
+    version = "v25.3",
+)
+
 HERMETIC_CC_TOOLCHAIN_VERSION = "v3.0.1"

 http_archive(
@@ -137,10 +165,10 @@ http_archive(
        # Expose internals of go_test for custom build transitions.
        "//third_party:io_bazel_rules_go_test.patch",
    ],
-    sha256 = "80a98277ad1311dacd837f9b16db62887702e9f1d1c4c9f796d0121a46c8e184",
+    sha256 = "b2038e2de2cace18f032249cb4bb0048abf583a36369fa98f687af1b3f880b26",
    urls = [
-        "https://mirror.bazel.build/github.com/bazelbuild/rules_go/releases/download/v0.46.0/rules_go-v0.46.0.zip",
-        "https://github.com/bazelbuild/rules_go/releases/download/v0.46.0/rules_go-v0.46.0.zip",
+        "https://mirror.bazel.build/github.com/bazelbuild/rules_go/releases/download/v0.48.1/rules_go-v0.48.1.zip",
+        "https://github.com/bazelbuild/rules_go/releases/download/v0.48.1/rules_go-v0.48.1.zip",
    ],
 )

@@ -182,7 +210,7 @@ load("@io_bazel_rules_go//go:deps.bzl", "go_register_toolchains", "go_rules_depe
 go_rules_dependencies()

 go_register_toolchains(
-    go_version = "1.22.10",
+    go_version = "1.23.5",
    nogo = "@//:nogo",
 )

@@ -227,7 +255,7 @@ filegroup(
    url = "https://github.com/ethereum/EIPs/archive/5480440fe51742ed23342b68cf106cefd427e39d.tar.gz",
 )

-consensus_spec_version = "v1.5.0-beta.0"
+consensus_spec_version = "v1.5.0-beta.2"

 bls_test_version = "v0.1.1"

@@ -243,7 +271,7 @@ filegroup(
    visibility = ["//visibility:public"],
 )
    """,
-    integrity = "sha256-HdMlTN3wv+hUMCkIRPk+EHcLixY1cSZlvkx3obEp4AM=",
+    integrity = "sha256-X/bMxbKg1clo2aFEjBoeuFq/U+BF1eQopgRP/7nI3Qg=",
    url = "https://github.com/ethereum/consensus-spec-tests/releases/download/%s/general.tar.gz" % consensus_spec_version,
 )

@@ -259,7 +287,7 @@ filegroup(
    visibility = ["//visibility:public"],
 )
    """,
-    integrity = "sha256-eX/ihmHQ+OvfoGJxSMgy22yAU3SZ3xjsX0FU0EaZrSs=",
+    integrity = "sha256-WSxdri5OJGuNApW+odKle5UzToDyEOx+F3lMiqamJAg=",
    url = "https://github.com/ethereum/consensus-spec-tests/releases/download/%s/minimal.tar.gz" % consensus_spec_version,
 )

@@ -275,7 +303,7 @@ filegroup(
    visibility = ["//visibility:public"],
 )
    """,
-    integrity = "sha256-k3Onf42vOzIqyddecR6G82sDy3mmDA+R8RN66QjB0GI=",
+    integrity = "sha256-LYE8l3y/zSt4YVrehrJ3ralqtgeYNildiIp+HR6+xAI=",
    url = "https://github.com/ethereum/consensus-spec-tests/releases/download/%s/mainnet.tar.gz" % consensus_spec_version,
 )

@@ -290,7 +318,7 @@ filegroup(
    visibility = ["//visibility:public"],
 )
    """,
-    integrity = "sha256-N/d4AwdOSlb70Dr+2l20dfXxNSzJDj/qKA9Rkn8Gb5w=",
+    integrity = "sha256-jvZQ90qcJMTOqMsPO7sgeEVQmewZTHcz7LVDkNqwTFQ=",
    strip_prefix = "consensus-specs-" + consensus_spec_version[1:],
    url = "https://github.com/ethereum/consensus-specs/archive/refs/tags/%s.tar.gz" % consensus_spec_version,
 )
--- a/api/client/beacon/BUILD.bazel
+++ b/api/client/beacon/BUILD.bazel
@@ -3,7 +3,6 @@ load("@prysm//tools/go:def.bzl", "go_library", "go_test")
 go_library(
    name = "go_default_library",
    srcs = [
-        "checkpoint.go",
        "client.go",
        "doc.go",
        "health.go",
@@ -16,28 +15,19 @@ go_library(
        "//api/client/beacon/iface:go_default_library",
        "//api/server:go_default_library",
        "//api/server/structs:go_default_library",
-        "//beacon-chain/core/helpers:go_default_library",
-        "//beacon-chain/state:go_default_library",
-        "//consensus-types/interfaces:go_default_library",
        "//consensus-types/primitives:go_default_library",
        "//encoding/bytesutil:go_default_library",
-        "//encoding/ssz/detect:go_default_library",
-        "//io/file:go_default_library",
        "//network/forks:go_default_library",
        "//proto/prysm/v1alpha1:go_default_library",
-        "//runtime/version:go_default_library",
-        "//time/slots:go_default_library",
        "@com_github_ethereum_go_ethereum//common/hexutil:go_default_library",
        "@com_github_pkg_errors//:go_default_library",
        "@com_github_sirupsen_logrus//:go_default_library",
-        "@org_golang_x_mod//semver:go_default_library",
    ],
 )

 go_test(
    name = "go_default_test",
    srcs = [
-        "checkpoint_test.go",
        "client_test.go",
        "health_test.go",
    ],
@@ -45,19 +35,7 @@ go_test(
    deps = [
        "//api/client:go_default_library",
        "//api/client/beacon/testing:go_default_library",
-        "//beacon-chain/state:go_default_library",
-        "//config/params:go_default_library",
-        "//consensus-types/blocks:go_default_library",
-        "//consensus-types/blocks/testing:go_default_library",
-        "//consensus-types/primitives:go_default_library",
-        "//encoding/ssz/detect:go_default_library",
-        "//network/forks:go_default_library",
-        "//proto/prysm/v1alpha1:go_default_library",
-        "//runtime/version:go_default_library",
        "//testing/require:go_default_library",
-        "//testing/util:go_default_library",
-        "//time/slots:go_default_library",
-        "@com_github_pkg_errors//:go_default_library",
        "@org_uber_go_mock//gomock:go_default_library",
    ],
 )
--- a/api/client/beacon/checkpoint.go
+++ b/api/client/beacon/checkpoint.go
@@ -1,276 +0,0 @@
-package beacon
-
-import (
-	"context"
-	"fmt"
-	"path"
-
-	"github.com/ethereum/go-ethereum/common/hexutil"
-	"github.com/pkg/errors"
-	base "github.com/prysmaticlabs/prysm/v5/api/client"
-	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
-	"github.com/prysmaticlabs/prysm/v5/beacon-chain/state"
-	"github.com/prysmaticlabs/prysm/v5/consensus-types/interfaces"
-	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
-	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
-	"github.com/prysmaticlabs/prysm/v5/encoding/ssz/detect"
-	"github.com/prysmaticlabs/prysm/v5/io/file"
-	"github.com/prysmaticlabs/prysm/v5/runtime/version"
-	"github.com/prysmaticlabs/prysm/v5/time/slots"
-	"github.com/sirupsen/logrus"
-	"golang.org/x/mod/semver"
-)
-
-var errCheckpointBlockMismatch = errors.New("mismatch between checkpoint sync state and block")
-
-// OriginData represents the BeaconState and ReadOnlySignedBeaconBlock necessary to start an empty Beacon Node
-// using Checkpoint Sync.
-type OriginData struct {
-	sb []byte
-	bb []byte
-	st state.BeaconState
-	b  interfaces.ReadOnlySignedBeaconBlock
-	vu *detect.VersionedUnmarshaler
-	br [32]byte
-	sr [32]byte
-}
-
-// SaveBlock saves the downloaded block to a unique file in the given path.
-// For readability and collision avoidance, the file name includes: type, config name, slot and root
-func (o *OriginData) SaveBlock(dir string) (string, error) {
-	blockPath := path.Join(dir, fname("block", o.vu, o.b.Block().Slot(), o.br))
-	return blockPath, file.WriteFile(blockPath, o.BlockBytes())
-}
-
-// SaveState saves the downloaded state to a unique file in the given path.
-// For readability and collision avoidance, the file name includes: type, config name, slot and root
-func (o *OriginData) SaveState(dir string) (string, error) {
-	statePath := path.Join(dir, fname("state", o.vu, o.st.Slot(), o.sr))
-	return statePath, file.WriteFile(statePath, o.StateBytes())
-}
-
-// StateBytes returns the ssz-encoded bytes of the downloaded BeaconState value.
-func (o *OriginData) StateBytes() []byte {
-	return o.sb
-}
-
-// BlockBytes returns the ssz-encoded bytes of the downloaded ReadOnlySignedBeaconBlock value.
-func (o *OriginData) BlockBytes() []byte {
-	return o.bb
-}
-
-func fname(prefix string, vu *detect.VersionedUnmarshaler, slot primitives.Slot, root [32]byte) string {
-	return fmt.Sprintf("%s_%s_%s_%d-%#x.ssz", prefix, vu.Config.ConfigName, version.String(vu.Fork), slot, root)
-}
-
-// DownloadFinalizedData downloads the most recently finalized state, and the block most recently applied to that state.
-// This pair can be used to initialize a new beacon node via checkpoint sync.
-func DownloadFinalizedData(ctx context.Context, client *Client) (*OriginData, error) {
-	sb, err := client.GetState(ctx, IdFinalized)
-	if err != nil {
-		return nil, err
-	}
-	vu, err := detect.FromState(sb)
-	if err != nil {
-		return nil, errors.Wrap(err, "error detecting chain config for finalized state")
-	}
-
-	log.WithFields(logrus.Fields{
-		"name": vu.Config.ConfigName,
-		"fork": version.String(vu.Fork),
-	}).Info("Detected supported config in remote finalized state")
-
-	s, err := vu.UnmarshalBeaconState(sb)
-	if err != nil {
-		return nil, errors.Wrap(err, "error unmarshaling finalized state to correct version")
-	}
-
-	slot := s.LatestBlockHeader().Slot
-	bb, err := client.GetBlock(ctx, IdFromSlot(slot))
-	if err != nil {
-		return nil, errors.Wrapf(err, "error requesting block by slot = %d", slot)
-	}
-	b, err := vu.UnmarshalBeaconBlock(bb)
-	if err != nil {
-		return nil, errors.Wrap(err, "unable to unmarshal block to a supported type using the detected fork schedule")
-	}
-	br, err := b.Block().HashTreeRoot()
-	if err != nil {
-		return nil, errors.Wrap(err, "error computing hash_tree_root of retrieved block")
-	}
-	bodyRoot, err := b.Block().Body().HashTreeRoot()
-	if err != nil {
-		return nil, errors.Wrap(err, "error computing hash_tree_root of retrieved block body")
-	}
-
-	sbr := bytesutil.ToBytes32(s.LatestBlockHeader().BodyRoot)
-	if sbr != bodyRoot {
-		return nil, errors.Wrapf(errCheckpointBlockMismatch, "state body root = %#x, block body root = %#x", sbr, bodyRoot)
-	}
-	sr, err := s.HashTreeRoot(ctx)
-	if err != nil {
-		return nil, errors.Wrapf(err, "failed to compute htr for finalized state at slot=%d", s.Slot())
-	}
-
-	log.
-		WithField("blockSlot", b.Block().Slot()).
-		WithField("stateSlot", s.Slot()).
-		WithField("stateRoot", hexutil.Encode(sr[:])).
-		WithField("blockRoot", hexutil.Encode(br[:])).
-		Info("Downloaded checkpoint sync state and block.")
-	return &OriginData{
-		st: s,
-		b:  b,
-		sb: sb,
-		bb: bb,
-		vu: vu,
-		br: br,
-		sr: sr,
-	}, nil
-}
-
-// WeakSubjectivityData represents the state root, block root and epoch of the BeaconState + ReadOnlySignedBeaconBlock
-// that falls at the beginning of the current weak subjectivity period. These values can be used to construct
-// a weak subjectivity checkpoint beacon node flag to be used for validation.
-type WeakSubjectivityData struct {
-	BlockRoot [32]byte
-	StateRoot [32]byte
-	Epoch     primitives.Epoch
-}
-
-// CheckpointString returns the standard string representation of a Checkpoint.
-// The format is a hex-encoded block root, followed by the epoch of the block, separated by a colon. For example:
-// "0x1c35540cac127315fabb6bf29181f2ae0de1a3fc909d2e76ba771e61312cc49a:74888"
-func (wsd *WeakSubjectivityData) CheckpointString() string {
-	return fmt.Sprintf("%#x:%d", wsd.BlockRoot, wsd.Epoch)
-}
-
-// ComputeWeakSubjectivityCheckpoint attempts to use the prysm weak_subjectivity api
-// to obtain the current weak_subjectivity checkpoint.
-// For non-prysm nodes, the same computation will be performed with extra steps,
-// using the head state downloaded from the beacon node api.
-func ComputeWeakSubjectivityCheckpoint(ctx context.Context, client *Client) (*WeakSubjectivityData, error) {
-	ws, err := client.GetWeakSubjectivity(ctx)
-	if err != nil {
-		// a 404/405 is expected if querying an endpoint that doesn't support the weak subjectivity checkpoint api
-		if !errors.Is(err, base.ErrNotOK) {
-			return nil, errors.Wrap(err, "unexpected API response for prysm-only weak subjectivity checkpoint API")
-		}
-		// fall back to vanilla Beacon Node API method
-		return computeBackwardsCompatible(ctx, client)
-	}
-	log.Printf("server weak subjectivity checkpoint response - epoch=%d, block_root=%#x, state_root=%#x", ws.Epoch, ws.BlockRoot, ws.StateRoot)
-	return ws, nil
-}
-
-const (
-	prysmMinimumVersion     = "v2.0.7"
-	prysmImplementationName = "Prysm"
-)
-
-// errUnsupportedPrysmCheckpointVersion indicates remote beacon node can't be used for checkpoint retrieval.
-var errUnsupportedPrysmCheckpointVersion = errors.New("node does not meet minimum version requirements for checkpoint retrieval")
-
-// for older endpoints or clients that do not support the weak_subjectivity api method
-// we gather the necessary data for a checkpoint sync by:
-// - inspecting the remote server's head state and computing the weak subjectivity epoch locally
-// - requesting the state at the first slot of the epoch
-// - using hash_tree_root(state.latest_block_header) to compute the block the state integrates
-// - requesting that block by its root
-func computeBackwardsCompatible(ctx context.Context, client *Client) (*WeakSubjectivityData, error) {
-	log.Print("falling back to generic checkpoint derivation, weak_subjectivity API not supported by server")
-	nv, err := client.GetNodeVersion(ctx)
-	if err != nil {
-		return nil, errors.Wrap(err, "unable to proceed with fallback method without confirming node version")
-	}
-	if nv.implementation == prysmImplementationName && semver.Compare(nv.semver, prysmMinimumVersion) < 0 {
-		return nil, errors.Wrapf(errUnsupportedPrysmCheckpointVersion, "%s < minimum (%s)", nv.semver, prysmMinimumVersion)
-	}
-	epoch, err := getWeakSubjectivityEpochFromHead(ctx, client)
-	if err != nil {
-		return nil, errors.Wrap(err, "error computing weak subjectivity epoch via head state inspection")
-	}
-
-	// use first slot of the epoch for the state slot
-	slot, err := slots.EpochStart(epoch)
-	if err != nil {
-		return nil, errors.Wrapf(err, "error computing first slot of epoch=%d", epoch)
-	}
-
-	log.Printf("requesting checkpoint state at slot %d", slot)
-	// get the state at the first slot of the epoch
-	sb, err := client.GetState(ctx, IdFromSlot(slot))
-	if err != nil {
-		return nil, errors.Wrapf(err, "failed to request state by slot from api, slot=%d", slot)
-	}
-
-	// ConfigFork is used to unmarshal the BeaconState so we can read the block root in latest_block_header
-	vu, err := detect.FromState(sb)
-	if err != nil {
-		return nil, errors.Wrap(err, "error detecting chain config for beacon state")
-	}
-	log.Printf("detected supported config in checkpoint state, name=%s, fork=%s", vu.Config.ConfigName, version.String(vu.Fork))
-
-	s, err := vu.UnmarshalBeaconState(sb)
-	if err != nil {
-		return nil, errors.Wrap(err, "error using detected config fork to unmarshal state bytes")
-	}
-
-	// compute state and block roots
-	sr, err := s.HashTreeRoot(ctx)
-	if err != nil {
-		return nil, errors.Wrap(err, "error computing hash_tree_root of state")
-	}
-
-	h := s.LatestBlockHeader()
-	h.StateRoot = sr[:]
-	br, err := h.HashTreeRoot()
-	if err != nil {
-		return nil, errors.Wrap(err, "error while computing block root using state data")
-	}
-
-	bb, err := client.GetBlock(ctx, IdFromRoot(br))
-	if err != nil {
-		return nil, errors.Wrapf(err, "error requesting block by root = %d", br)
-	}
-	b, err := vu.UnmarshalBeaconBlock(bb)
-	if err != nil {
-		return nil, errors.Wrap(err, "unable to unmarshal block to a supported type using the detected fork schedule")
-	}
-	br, err = b.Block().HashTreeRoot()
-	if err != nil {
-		return nil, errors.Wrap(err, "error computing hash_tree_root for block obtained via root")
-	}
-
-	return &WeakSubjectivityData{
-		Epoch:     epoch,
-		BlockRoot: br,
-		StateRoot: sr,
-	}, nil
-}
-
-// this method downloads the head state, which can be used to find the correct chain config
-// and use prysm's helper methods to compute the latest weak subjectivity epoch.
-func getWeakSubjectivityEpochFromHead(ctx context.Context, client *Client) (primitives.Epoch, error) {
-	headBytes, err := client.GetState(ctx, IdHead)
-	if err != nil {
-		return 0, err
-	}
-	vu, err := detect.FromState(headBytes)
-	if err != nil {
-		return 0, errors.Wrap(err, "error detecting chain config for beacon state")
-	}
-	log.Printf("detected supported config in remote head state, name=%s, fork=%s", vu.Config.ConfigName, version.String(vu.Fork))
-	headState, err := vu.UnmarshalBeaconState(headBytes)
-	if err != nil {
-		return 0, errors.Wrap(err, "error unmarshaling state to correct version")
-	}
-
-	epoch, err := helpers.LatestWeakSubjectivityEpoch(ctx, headState, vu.Config)
-	if err != nil {
-		return 0, errors.Wrap(err, "error computing the weak subjectivity epoch from head state")
-	}
-
-	log.Printf("(computed client-side) weak subjectivity epoch = %d", epoch)
-	return epoch, nil
-}
--- a/api/client/beacon/client.go
+++ b/api/client/beacon/client.go
@@ -29,12 +29,13 @@ const (
 	getSignedBlockPath       = "/eth/v2/beacon/blocks"
 	getBlockRootPath         = "/eth/v1/beacon/blocks/{{.Id}}/root"
 	getForkForStatePath      = "/eth/v1/beacon/states/{{.Id}}/fork"
-	getWeakSubjectivityPath  = "/prysm/v1/beacon/weak_subjectivity"
 	getForkSchedulePath      = "/eth/v1/config/fork_schedule"
 	getConfigSpecPath        = "/eth/v1/config/spec"
 	getStatePath             = "/eth/v2/debug/beacon/states"
-	getNodeVersionPath       = "/eth/v1/node/version"
 	changeBLStoExecutionPath = "/eth/v1/beacon/pool/bls_to_execution_changes"
+
+	GetNodeVersionPath      = "/eth/v1/node/version"
+	GetWeakSubjectivityPath = "/prysm/v1/beacon/weak_subjectivity"
 )

 // StateOrBlockId represents the block_id / state_id parameters that several of the Eth Beacon API methods accept.
@@ -80,7 +81,8 @@ func idTemplate(ts string) func(StateOrBlockId) string {
 	return f
 }

-func renderGetBlockPath(id StateOrBlockId) string {
+// RenderGetBlockPath formats a block id into a path for the GetBlock API endpoint.
+func RenderGetBlockPath(id StateOrBlockId) string {
 	return path.Join(getSignedBlockPath, string(id))
 }

@@ -104,7 +106,7 @@ func NewClient(host string, opts ...client.ClientOpt) (*Client, error) {
 // for the named identifiers.
 // The return value contains the ssz-encoded bytes.
 func (c *Client) GetBlock(ctx context.Context, blockId StateOrBlockId) ([]byte, error) {
-	blockPath := renderGetBlockPath(blockId)
+	blockPath := RenderGetBlockPath(blockId)
 	b, err := c.Get(ctx, blockPath, client.WithSSZEncoding())
 	if err != nil {
 		return nil, errors.Wrapf(err, "error requesting state by id = %s", blockId)
@@ -195,6 +197,10 @@ type NodeVersion struct {
 	systemInfo     string
 }

+func (nv *NodeVersion) SetImplementation(impl string) {
+	nv.implementation = impl
+}
+
 var versionRE = regexp.MustCompile(`^(\w+)/(v\d+\.\d+\.\d+[-a-zA-Z0-9]*)\s*/?(.*)$`)

 func parseNodeVersion(v string) (*NodeVersion, error) {
@@ -212,7 +218,7 @@ func parseNodeVersion(v string) (*NodeVersion, error) {
 // GetNodeVersion requests that the beacon node identify information about its implementation in a format
 // similar to a HTTP User-Agent field. ex: Lighthouse/v0.1.5 (Linux x86_64)
 func (c *Client) GetNodeVersion(ctx context.Context) (*NodeVersion, error) {
-	b, err := c.Get(ctx, getNodeVersionPath)
+	b, err := c.Get(ctx, GetNodeVersionPath)
 	if err != nil {
 		return nil, errors.Wrap(err, "error requesting node version")
 	}
@@ -228,7 +234,8 @@ func (c *Client) GetNodeVersion(ctx context.Context) (*NodeVersion, error) {
 	return parseNodeVersion(d.Data.Version)
 }

-func renderGetStatePath(id StateOrBlockId) string {
+// RenderGetStatePath formats a state id into a path for the GetState API endpoint.
+func RenderGetStatePath(id StateOrBlockId) string {
 	return path.Join(getStatePath, string(id))
 }

@@ -246,13 +253,29 @@ func (c *Client) GetState(ctx context.Context, stateId StateOrBlockId) ([]byte,
 	return b, nil
 }

+// WeakSubjectivityData represents the state root, block root and epoch of the BeaconState + ReadOnlySignedBeaconBlock
+// that falls at the beginning of the current weak subjectivity period. These values can be used to construct
+// a weak subjectivity checkpoint beacon node flag to be used for validation.
+type WeakSubjectivityData struct {
+	BlockRoot [32]byte
+	StateRoot [32]byte
+	Epoch     primitives.Epoch
+}
+
+// CheckpointString returns the standard string representation of a Checkpoint.
+// The format is a hex-encoded block root, followed by the epoch of the block, separated by a colon. For example:
+// "0x1c35540cac127315fabb6bf29181f2ae0de1a3fc909d2e76ba771e61312cc49a:74888"
+func (wsd *WeakSubjectivityData) CheckpointString() string {
+	return fmt.Sprintf("%#x:%d", wsd.BlockRoot, wsd.Epoch)
+}
+
 // GetWeakSubjectivity calls a proposed API endpoint that is unique to prysm
 // This api method does the following:
 // - computes weak subjectivity epoch
 // - finds the highest non-skipped block preceding the epoch
 // - returns the htr of the found block and returns this + the value of state_root from the block
 func (c *Client) GetWeakSubjectivity(ctx context.Context) (*WeakSubjectivityData, error) {
-	body, err := c.Get(ctx, getWeakSubjectivityPath)
+	body, err := c.Get(ctx, GetWeakSubjectivityPath)
 	if err != nil {
 		return nil, err
 	}
--- a/api/client/beacon/client_test.go
+++ b/api/client/beacon/client_test.go
@@ -97,31 +97,31 @@ func TestValidHostname(t *testing.T) {
 		{
 			name:    "hostname with port",
 			hostArg: "mydomain.org:3500",
-			path:    getNodeVersionPath,
+			path:    GetNodeVersionPath,
 			joined:  "http://mydomain.org:3500/eth/v1/node/version",
 		},
 		{
 			name:    "https scheme, hostname with port",
 			hostArg: "https://mydomain.org:3500",
-			path:    getNodeVersionPath,
+			path:    GetNodeVersionPath,
 			joined:  "https://mydomain.org:3500/eth/v1/node/version",
 		},
 		{
 			name:    "http scheme, hostname without port",
 			hostArg: "http://mydomain.org",
-			path:    getNodeVersionPath,
+			path:    GetNodeVersionPath,
 			joined:  "http://mydomain.org/eth/v1/node/version",
 		},
 		{
 			name:    "http scheme, trailing slash, hostname without port",
 			hostArg: "http://mydomain.org/",
-			path:    getNodeVersionPath,
+			path:    GetNodeVersionPath,
 			joined:  "http://mydomain.org/eth/v1/node/version",
 		},
 		{
 			name:    "http scheme, hostname with basic auth creds and no port",
 			hostArg: "http://username:pass@mydomain.org/",
-			path:    getNodeVersionPath,
+			path:    GetNodeVersionPath,
 			joined:  "http://username:pass@mydomain.org/eth/v1/node/version",
 		},
 	}
--- a/api/client/builder/BUILD.bazel
+++ b/api/client/builder/BUILD.bazel
@@ -13,6 +13,7 @@ go_library(
    deps = [
        "//api:go_default_library",
        "//api/client:go_default_library",
+        "//api/server:go_default_library",
        "//api/server/structs:go_default_library",
        "//config/fieldparams:go_default_library",
        "//config/params:go_default_library",
@@ -27,6 +28,7 @@ go_library(
        "//proto/engine/v1:go_default_library",
        "//proto/prysm/v1alpha1:go_default_library",
        "//runtime/version:go_default_library",
+        "@com_github_ethereum_go_ethereum//common:go_default_library",
        "@com_github_ethereum_go_ethereum//common/hexutil:go_default_library",
        "@com_github_pkg_errors//:go_default_library",
        "@com_github_prysmaticlabs_fastssz//:go_default_library",
--- a/api/client/builder/bid.go
+++ b/api/client/builder/bid.go
@@ -1,12 +1,12 @@
 package builder

 import (
-	"github.com/pkg/errors"
 	ssz "github.com/prysmaticlabs/fastssz"
 	consensus_types "github.com/prysmaticlabs/prysm/v5/consensus-types"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/interfaces"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	v1 "github.com/prysmaticlabs/prysm/v5/proto/engine/v1"
 	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
 	"github.com/prysmaticlabs/prysm/v5/runtime/version"
 )
@@ -22,7 +22,6 @@ type SignedBid interface {
 // Bid is an interface describing the method set of a builder bid.
 type Bid interface {
 	Header() (interfaces.ExecutionData, error)
-	BlobKzgCommitments() ([][]byte, error)
 	Value() primitives.Wei
 	Pubkey() []byte
 	Version() int
@@ -31,6 +30,18 @@ type Bid interface {
 	HashTreeRootWith(hh *ssz.Hasher) error
 }

+// BidDeneb is an interface that exposes newly added kzg commitments on top of builder bid
+type BidDeneb interface {
+	Bid
+	BlobKzgCommitments() [][]byte
+}
+
+// BidElectra is an interface that exposes the newly added execution requests on top of the builder bid
+type BidElectra interface {
+	BidDeneb
+	ExecutionRequests() *v1.ExecutionRequests
+}
+
 type signedBuilderBid struct {
 	p *ethpb.SignedBuilderBid
 }
@@ -115,11 +126,6 @@ func (b builderBid) Header() (interfaces.ExecutionData, error) {
 	return blocks.WrappedExecutionPayloadHeader(b.p.Header)
 }

-// BlobKzgCommitments --
-func (b builderBid) BlobKzgCommitments() ([][]byte, error) {
-	return [][]byte{}, errors.New("blob kzg commitments not available before Deneb")
-}
-
 // Version --
 func (b builderBid) Version() int {
 	return version.Bellatrix
@@ -169,11 +175,6 @@ func (b builderBidCapella) Header() (interfaces.ExecutionData, error) {
 	return blocks.WrappedExecutionPayloadHeaderCapella(b.p.Header)
 }

-// BlobKzgCommitments --
-func (b builderBidCapella) BlobKzgCommitments() ([][]byte, error) {
-	return [][]byte{}, errors.New("blob kzg commitments not available before Deneb")
-}
-
 // Version --
 func (b builderBidCapella) Version() int {
 	return version.Capella
@@ -254,8 +255,8 @@ func (b builderBidDeneb) Header() (interfaces.ExecutionData, error) {
 }

 // BlobKzgCommitments --
-func (b builderBidDeneb) BlobKzgCommitments() ([][]byte, error) {
-	return b.p.BlobKzgCommitments, nil
+func (b builderBidDeneb) BlobKzgCommitments() [][]byte {
+	return b.p.BlobKzgCommitments
 }

 type signedBuilderBidDeneb struct {
@@ -290,3 +291,95 @@ func (b signedBuilderBidDeneb) Version() int {
 func (b signedBuilderBidDeneb) IsNil() bool {
 	return b.p == nil
 }
+
+type builderBidElectra struct {
+	p *ethpb.BuilderBidElectra
+}
+
+// WrappedBuilderBidElectra is a constructor which wraps a protobuf bid into an interface.
+func WrappedBuilderBidElectra(p *ethpb.BuilderBidElectra) (Bid, error) {
+	w := builderBidElectra{p: p}
+	if w.IsNil() {
+		return nil, consensus_types.ErrNilObjectWrapped
+	}
+	return w, nil
+}
+
+// Version --
+func (b builderBidElectra) Version() int {
+	return version.Electra
+}
+
+// Value --
+func (b builderBidElectra) Value() primitives.Wei {
+	return primitives.LittleEndianBytesToWei(b.p.Value)
+}
+
+// Pubkey --
+func (b builderBidElectra) Pubkey() []byte {
+	return b.p.Pubkey
+}
+
+// IsNil --
+func (b builderBidElectra) IsNil() bool {
+	return b.p == nil
+}
+
+// HashTreeRoot --
+func (b builderBidElectra) HashTreeRoot() ([32]byte, error) {
+	return b.p.HashTreeRoot()
+}
+
+// HashTreeRootWith --
+func (b builderBidElectra) HashTreeRootWith(hh *ssz.Hasher) error {
+	return b.p.HashTreeRootWith(hh)
+}
+
+// Header --
+func (b builderBidElectra) Header() (interfaces.ExecutionData, error) {
+	// We have to convert big endian to little endian because the value is coming from the execution layer.
+	return blocks.WrappedExecutionPayloadHeaderDeneb(b.p.Header)
+}
+
+// ExecutionRequests --
+func (b builderBidElectra) ExecutionRequests() *v1.ExecutionRequests {
+	return b.p.ExecutionRequests // does not copy
+}
+
+// BlobKzgCommitments --
+func (b builderBidElectra) BlobKzgCommitments() [][]byte {
+	return b.p.BlobKzgCommitments
+}
+
+type signedBuilderBidElectra struct {
+	p *ethpb.SignedBuilderBidElectra
+}
+
+// WrappedSignedBuilderBidElectra is a constructor which wraps a protobuf signed bit into an interface.
+func WrappedSignedBuilderBidElectra(p *ethpb.SignedBuilderBidElectra) (SignedBid, error) {
+	w := signedBuilderBidElectra{p: p}
+	if w.IsNil() {
+		return nil, consensus_types.ErrNilObjectWrapped
+	}
+	return w, nil
+}
+
+// Message --
+func (b signedBuilderBidElectra) Message() (Bid, error) {
+	return WrappedBuilderBidElectra(b.p.Message)
+}
+
+// Signature --
+func (b signedBuilderBidElectra) Signature() []byte {
+	return b.p.Signature
+}
+
+// Version --
+func (b signedBuilderBidElectra) Version() int {
+	return version.Electra
+}
+
+// IsNil --
+func (b signedBuilderBidElectra) IsNil() bool {
+	return b.p == nil
+}
--- a/api/client/builder/client.go
+++ b/api/client/builder/client.go
@@ -219,8 +219,23 @@ func (c *Client) GetHeader(ctx context.Context, slot primitives.Slot, parentHash
 	if err := json.Unmarshal(hb, v); err != nil {
 		return nil, errors.Wrapf(err, "error unmarshaling the builder GetHeader response, using slot=%d, parentHash=%#x, pubkey=%#x", slot, parentHash, pubkey)
 	}
-	switch strings.ToLower(v.Version) {
-	case strings.ToLower(version.String(version.Deneb)):
+
+	ver, err := version.FromString(strings.ToLower(v.Version))
+	if err != nil {
+		return nil, errors.Wrap(err, fmt.Sprintf("unsupported header version %s", strings.ToLower(v.Version)))
+	}
+	if ver >= version.Electra {
+		hr := &ExecHeaderResponseElectra{}
+		if err := json.Unmarshal(hb, hr); err != nil {
+			return nil, errors.Wrapf(err, "error unmarshaling the builder GetHeader response, using slot=%d, parentHash=%#x, pubkey=%#x", slot, parentHash, pubkey)
+		}
+		p, err := hr.ToProto()
+		if err != nil {
+			return nil, errors.Wrapf(err, "could not extract proto message from header")
+		}
+		return WrappedSignedBuilderBidElectra(p)
+	}
+	if ver >= version.Deneb {
 		hr := &ExecHeaderResponseDeneb{}
 		if err := json.Unmarshal(hb, hr); err != nil {
 			return nil, errors.Wrapf(err, "error unmarshaling the builder GetHeader response, using slot=%d, parentHash=%#x, pubkey=%#x", slot, parentHash, pubkey)
@@ -230,7 +245,8 @@ func (c *Client) GetHeader(ctx context.Context, slot primitives.Slot, parentHash
 			return nil, errors.Wrapf(err, "could not extract proto message from header")
 		}
 		return WrappedSignedBuilderBidDeneb(p)
-	case strings.ToLower(version.String(version.Capella)):
+	}
+	if ver >= version.Capella {
 		hr := &ExecHeaderResponseCapella{}
 		if err := json.Unmarshal(hb, hr); err != nil {
 			return nil, errors.Wrapf(err, "error unmarshaling the builder GetHeader response, using slot=%d, parentHash=%#x, pubkey=%#x", slot, parentHash, pubkey)
@@ -240,7 +256,8 @@ func (c *Client) GetHeader(ctx context.Context, slot primitives.Slot, parentHash
 			return nil, errors.Wrapf(err, "could not extract proto message from header")
 		}
 		return WrappedSignedBuilderBidCapella(p)
-	case strings.ToLower(version.String(version.Bellatrix)):
+	}
+	if ver >= version.Bellatrix {
 		hr := &ExecHeaderResponse{}
 		if err := json.Unmarshal(hb, hr); err != nil {
 			return nil, errors.Wrapf(err, "error unmarshaling the builder GetHeader response, using slot=%d, parentHash=%#x, pubkey=%#x", slot, parentHash, pubkey)
@@ -250,9 +267,8 @@ func (c *Client) GetHeader(ctx context.Context, slot primitives.Slot, parentHash
 			return nil, errors.Wrap(err, "could not extract proto message from header")
 		}
 		return WrappedSignedBuilderBid(p)
-	default:
-		return nil, fmt.Errorf("unsupported header version %s", strings.ToLower(v.Version))
 	}
+	return nil, fmt.Errorf("unsupported header version %s", strings.ToLower(v.Version))
 }

 // RegisterValidator encodes the SignedValidatorRegistrationV1 message to json (including hex-encoding the byte
--- a/api/client/builder/client_test.go
+++ b/api/client/builder/client_test.go
@@ -266,9 +266,9 @@ func TestClient_GetHeader(t *testing.T) {
 		require.NoError(t, err)
 		require.Equal(t, 0, value.Int.Cmp(primitives.WeiToBigInt(bid.Value())))
 		require.Equal(t, bidStr, primitives.WeiToBigInt(bid.Value()).String())
-
-		kcgCommitments, err := bid.BlobKzgCommitments()
-		require.NoError(t, err)
+		dbid, ok := bid.(builderBidDeneb)
+		require.Equal(t, true, ok)
+		kcgCommitments := dbid.BlobKzgCommitments()
 		require.Equal(t, len(kcgCommitments) > 0, true)
 		for i := range kcgCommitments {
 			require.Equal(t, len(kcgCommitments[i]) == 48, true)
@@ -292,6 +292,50 @@ func TestClient_GetHeader(t *testing.T) {
 		_, err := c.GetHeader(ctx, slot, bytesutil.ToBytes32(parentHash), bytesutil.ToBytes48(pubkey))
 		require.ErrorContains(t, "could not extract proto message from header: too many blob commitments: 7", err)
 	})
+	t.Run("electra", func(t *testing.T) {
+		hc := &http.Client{
+			Transport: roundtrip(func(r *http.Request) (*http.Response, error) {
+				require.Equal(t, expectedPath, r.URL.Path)
+				return &http.Response{
+					StatusCode: http.StatusOK,
+					Body:       io.NopCloser(bytes.NewBufferString(testExampleHeaderResponseElectra)),
+					Request:    r.Clone(ctx),
+				}, nil
+			}),
+		}
+		c := &Client{
+			hc:      hc,
+			baseURL: &url.URL{Host: "localhost:3500", Scheme: "http"},
+		}
+		h, err := c.GetHeader(ctx, slot, bytesutil.ToBytes32(parentHash), bytesutil.ToBytes48(pubkey))
+		require.NoError(t, err)
+		expectedWithdrawalsRoot := ezDecode(t, "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2")
+		bid, err := h.Message()
+		require.NoError(t, err)
+		bidHeader, err := bid.Header()
+		require.NoError(t, err)
+		withdrawalsRoot, err := bidHeader.WithdrawalsRoot()
+		require.NoError(t, err)
+		require.Equal(t, true, bytes.Equal(expectedWithdrawalsRoot, withdrawalsRoot))
+
+		bidStr := "652312848583266388373324160190187140051835877600158453279131187530910662656"
+		value, err := stringToUint256(bidStr)
+		require.NoError(t, err)
+		require.Equal(t, 0, value.Int.Cmp(primitives.WeiToBigInt(bid.Value())))
+		require.Equal(t, bidStr, primitives.WeiToBigInt(bid.Value()).String())
+		ebid, ok := bid.(builderBidElectra)
+		require.Equal(t, true, ok)
+		kcgCommitments := ebid.BlobKzgCommitments()
+		require.Equal(t, len(kcgCommitments) > 0, true)
+		for i := range kcgCommitments {
+			require.Equal(t, len(kcgCommitments[i]) == 48, true)
+		}
+		requests := ebid.ExecutionRequests()
+		require.Equal(t, 1, len(requests.Deposits))
+		require.Equal(t, 1, len(requests.Withdrawals))
+		require.Equal(t, 1, len(requests.Consolidations))
+
+	})
 	t.Run("unsupported version", func(t *testing.T) {
 		hc := &http.Client{
 			Transport: roundtrip(func(r *http.Request) (*http.Response, error) {
--- a/api/client/builder/types.go
+++ b/api/client/builder/types.go
@@ -5,13 +5,15 @@ import (
 	"fmt"
 	"math/big"
 	"strconv"
+	"strings"

+	"github.com/ethereum/go-ethereum/common"
 	"github.com/ethereum/go-ethereum/common/hexutil"
 	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/api/server"
 	fieldparams "github.com/prysmaticlabs/prysm/v5/config/fieldparams"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	consensusblocks "github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
-	"github.com/prysmaticlabs/prysm/v5/consensus-types/interfaces"
 	types "github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	"github.com/prysmaticlabs/prysm/v5/math"
@@ -414,54 +416,10 @@ func FromProtoDeneb(payload *v1.ExecutionPayloadDeneb) (ExecutionPayloadDeneb, e
 	}, nil
 }

-var errInvalidTypeConversion = errors.New("unable to translate between api and foreign type")
-
-// ExecutionPayloadResponseFromData converts an ExecutionData interface value to a payload response.
-// This involves serializing the execution payload value so that the abstract payload envelope can be used.
-func ExecutionPayloadResponseFromData(ed interfaces.ExecutionData, bundle *v1.BlobsBundle) (*ExecutionPayloadResponse, error) {
-	pb := ed.Proto()
-	var data interface{}
-	var err error
-	var ver string
-	switch pbStruct := pb.(type) {
-	case *v1.ExecutionPayload:
-		ver = version.String(version.Bellatrix)
-		data, err = FromProto(pbStruct)
-		if err != nil {
-			return nil, errors.Wrap(err, "failed to convert a Bellatrix ExecutionPayload to an API response")
-		}
-	case *v1.ExecutionPayloadCapella:
-		ver = version.String(version.Capella)
-		data, err = FromProtoCapella(pbStruct)
-		if err != nil {
-			return nil, errors.Wrap(err, "failed to convert a Capella ExecutionPayload to an API response")
-		}
-	case *v1.ExecutionPayloadDeneb:
-		ver = version.String(version.Deneb)
-		payloadStruct, err := FromProtoDeneb(pbStruct)
-		if err != nil {
-			return nil, errors.Wrap(err, "failed to convert a Deneb ExecutionPayload to an API response")
-		}
-		data = &ExecutionPayloadDenebAndBlobsBundle{
-			ExecutionPayload: &payloadStruct,
-			BlobsBundle:      FromBundleProto(bundle),
-		}
-	default:
-		return nil, errInvalidTypeConversion
-	}
-	encoded, err := json.Marshal(data)
-	if err != nil {
-		return nil, errors.Wrapf(err, "failed to marshal execution payload version=%s", ver)
-	}
-	return &ExecutionPayloadResponse{
-		Version: ver,
-		Data:    encoded,
-	}, nil
-}
-
 // ExecHeaderResponseCapella is the response of builder API /eth/v1/builder/header/{slot}/{parent_hash}/{pubkey} for Capella.
 type ExecHeaderResponseCapella struct {
-	Data struct {
+	Version string `json:"version"`
+	Data    struct {
 		Signature hexutil.Bytes      `json:"signature"`
 		Message   *BuilderBidCapella `json:"message"`
 	} `json:"data"`
@@ -605,17 +563,25 @@ type BlobBundler interface {
 	BundleProto() (*v1.BlobsBundle, error)
 }

+// ParsedExecutionRequests can retrieve the underlying execution requests for the given execution payload response.
+type ParsedExecutionRequests interface {
+	ExecutionRequestsProto() (*v1.ExecutionRequests, error)
+}
+
 func (r *ExecutionPayloadResponse) ParsePayload() (ParsedPayload, error) {
 	var toProto ParsedPayload
-	switch r.Version {
-	case version.String(version.Bellatrix):
-		toProto = &ExecutionPayload{}
-	case version.String(version.Capella):
-		toProto = &ExecutionPayloadCapella{}
-	case version.String(version.Deneb):
+	v, err := version.FromString(strings.ToLower(r.Version))
+	if err != nil {
+		return nil, errors.Wrap(err, fmt.Sprintf("unsupported version %s", strings.ToLower(r.Version)))
+	}
+	if v >= version.Deneb {
 		toProto = &ExecutionPayloadDenebAndBlobsBundle{}
-	default:
-		return nil, consensusblocks.ErrUnsupportedVersion
+	} else if v >= version.Capella {
+		toProto = &ExecutionPayloadCapella{}
+	} else if v >= version.Bellatrix {
+		toProto = &ExecutionPayload{}
+	} else {
+		return nil, fmt.Errorf("unsupported version %s", strings.ToLower(r.Version))
 	}

 	if err := json.Unmarshal(r.Data, toProto); err != nil {
@@ -990,7 +956,8 @@ func (ch *BLSToExecutionChange) MarshalJSON() ([]byte, error) {

 // ExecHeaderResponseDeneb is the header response for builder API /eth/v1/builder/header/{slot}/{parent_hash}/{pubkey}.
 type ExecHeaderResponseDeneb struct {
-	Data struct {
+	Version string `json:"version"`
+	Data    struct {
 		Signature hexutil.Bytes    `json:"signature"`
 		Message   *BuilderBidDeneb `json:"message"`
 	} `json:"data"`
@@ -1307,6 +1274,208 @@ func (p *ExecutionPayloadDeneb) ToProto() (*v1.ExecutionPayloadDeneb, error) {
 	}, nil
 }

+// ExecHeaderResponseElectra is the header response for builder API /eth/v1/builder/header/{slot}/{parent_hash}/{pubkey}.
+type ExecHeaderResponseElectra struct {
+	Version string `json:"version"`
+	Data    struct {
+		Signature hexutil.Bytes      `json:"signature"`
+		Message   *BuilderBidElectra `json:"message"`
+	} `json:"data"`
+}
+
+// ToProto creates a SignedBuilderBidElectra Proto from ExecHeaderResponseElectra.
+func (ehr *ExecHeaderResponseElectra) ToProto() (*eth.SignedBuilderBidElectra, error) {
+	bb, err := ehr.Data.Message.ToProto()
+	if err != nil {
+		return nil, err
+	}
+	return &eth.SignedBuilderBidElectra{
+		Message:   bb,
+		Signature: bytesutil.SafeCopyBytes(ehr.Data.Signature),
+	}, nil
+}
+
+// ToProto creates a BuilderBidElectra Proto from BuilderBidElectra.
+func (bb *BuilderBidElectra) ToProto() (*eth.BuilderBidElectra, error) {
+	header, err := bb.Header.ToProto()
+	if err != nil {
+		return nil, err
+	}
+	if len(bb.BlobKzgCommitments) > params.BeaconConfig().MaxBlobsPerBlockByVersion(version.Electra) {
+		return nil, fmt.Errorf("blob commitment count %d exceeds the maximum %d", len(bb.BlobKzgCommitments), params.BeaconConfig().MaxBlobsPerBlockByVersion(version.Electra))
+	}
+	kzgCommitments := make([][]byte, len(bb.BlobKzgCommitments))
+	for i, commit := range bb.BlobKzgCommitments {
+		if len(commit) != fieldparams.BLSPubkeyLength {
+			return nil, fmt.Errorf("commitment length %d is not %d", len(commit), fieldparams.BLSPubkeyLength)
+		}
+		kzgCommitments[i] = bytesutil.SafeCopyBytes(commit)
+	}
+	// post electra execution requests should not be nil, if no requests exist use an empty request
+	if bb.ExecutionRequests == nil {
+		return nil, errors.New("bid contains nil execution requests")
+	}
+	executionRequests, err := bb.ExecutionRequests.ToProto()
+	if err != nil {
+		return nil, errors.Wrap(err, "failed to convert ExecutionRequests")
+	}
+	return &eth.BuilderBidElectra{
+		Header:             header,
+		BlobKzgCommitments: kzgCommitments,
+		ExecutionRequests:  executionRequests,
+		// Note that SSZBytes() reverses byte order for the little-endian representation.
+		// Uint256.Bytes() is big-endian, SSZBytes takes this value and reverses it.
+		Value:  bytesutil.SafeCopyBytes(bb.Value.SSZBytes()),
+		Pubkey: bytesutil.SafeCopyBytes(bb.Pubkey),
+	}, nil
+}
+
+// ExecutionRequestsV1 is a wrapper for different execution requests
+type ExecutionRequestsV1 struct {
+	Deposits       []*DepositRequestV1       `json:"deposits"`
+	Withdrawals    []*WithdrawalRequestV1    `json:"withdrawals"`
+	Consolidations []*ConsolidationRequestV1 `json:"consolidations"`
+}
+
+func (er *ExecutionRequestsV1) ToProto() (*v1.ExecutionRequests, error) {
+	if uint64(len(er.Deposits)) > params.BeaconConfig().MaxDepositRequestsPerPayload {
+		return nil, fmt.Errorf("deposit requests count %d exceeds the maximum %d", len(er.Deposits), params.BeaconConfig().MaxDepositRequestsPerPayload)
+	}
+	deposits := make([]*v1.DepositRequest, len(er.Deposits))
+	for i, dep := range er.Deposits {
+		d, err := dep.ToProto()
+		if err != nil {
+			return nil, err
+		}
+		deposits[i] = d
+	}
+	if uint64(len(er.Withdrawals)) > params.BeaconConfig().MaxWithdrawalRequestsPerPayload {
+		return nil, fmt.Errorf("withdrawal requests count %d exceeds the maximum %d", len(er.Withdrawals), params.BeaconConfig().MaxWithdrawalRequestsPerPayload)
+	}
+	withdrawals := make([]*v1.WithdrawalRequest, len(er.Withdrawals))
+	for i, wr := range er.Withdrawals {
+		w, err := wr.ToProto()
+		if err != nil {
+			return nil, err
+		}
+		withdrawals[i] = w
+	}
+	if uint64(len(er.Consolidations)) > params.BeaconConfig().MaxConsolidationsRequestsPerPayload {
+		return nil, fmt.Errorf("consolidation requests count %d exceeds the maximum %d", len(er.Consolidations), params.BeaconConfig().MaxConsolidationsRequestsPerPayload)
+	}
+	consolidations := make([]*v1.ConsolidationRequest, len(er.Consolidations))
+	for i, con := range er.Consolidations {
+		c, err := con.ToProto()
+		if err != nil {
+			return nil, err
+		}
+		consolidations[i] = c
+	}
+	return &v1.ExecutionRequests{
+		Deposits:       deposits,
+		Withdrawals:    withdrawals,
+		Consolidations: consolidations,
+	}, nil
+}
+
+// BuilderBidElectra is a field of ExecHeaderResponseElectra.
+type BuilderBidElectra struct {
+	Header             *ExecutionPayloadHeaderDeneb `json:"header"`
+	BlobKzgCommitments []hexutil.Bytes              `json:"blob_kzg_commitments"`
+	ExecutionRequests  *ExecutionRequestsV1         `json:"execution_requests"`
+	Value              Uint256                      `json:"value"`
+	Pubkey             hexutil.Bytes                `json:"pubkey"`
+}
+
+// WithdrawalRequestV1 is a field of ExecutionRequestsV1.
+type WithdrawalRequestV1 struct {
+	SourceAddress   hexutil.Bytes `json:"source_address"`
+	ValidatorPubkey hexutil.Bytes `json:"validator_pubkey"`
+	Amount          Uint256       `json:"amount"`
+}
+
+func (wr *WithdrawalRequestV1) ToProto() (*v1.WithdrawalRequest, error) {
+	srcAddress, err := bytesutil.DecodeHexWithLength(wr.SourceAddress.String(), common.AddressLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "source_address")
+	}
+	pubkey, err := bytesutil.DecodeHexWithLength(wr.ValidatorPubkey.String(), fieldparams.BLSPubkeyLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "validator_pubkey")
+	}
+
+	return &v1.WithdrawalRequest{
+		SourceAddress:   srcAddress,
+		ValidatorPubkey: pubkey,
+		Amount:          wr.Amount.Uint64(),
+	}, nil
+}
+
+// DepositRequestV1 is a field of ExecutionRequestsV1.
+type DepositRequestV1 struct {
+	PubKey hexutil.Bytes `json:"pubkey"`
+	// withdrawalCredentials: DATA, 32 Bytes
+	WithdrawalCredentials hexutil.Bytes `json:"withdrawal_credentials"`
+	// amount: QUANTITY, 64 Bits
+	Amount Uint256 `json:"amount"`
+	// signature: DATA, 96 Bytes
+	Signature hexutil.Bytes `json:"signature"`
+	// index: QUANTITY, 64 Bits
+	Index Uint256 `json:"index"`
+}
+
+func (dr *DepositRequestV1) ToProto() (*v1.DepositRequest, error) {
+	pubkey, err := bytesutil.DecodeHexWithLength(dr.PubKey.String(), fieldparams.BLSPubkeyLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "pubkey")
+	}
+	wc, err := bytesutil.DecodeHexWithLength(dr.WithdrawalCredentials.String(), fieldparams.RootLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "withdrawal_credentials")
+	}
+	sig, err := bytesutil.DecodeHexWithLength(dr.Signature.String(), fieldparams.BLSSignatureLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "signature")
+	}
+	return &v1.DepositRequest{
+		Pubkey:                pubkey,
+		WithdrawalCredentials: wc,
+		Amount:                dr.Amount.Uint64(),
+		Signature:             sig,
+		Index:                 dr.Index.Uint64(),
+	}, nil
+}
+
+// ConsolidationRequestV1 is a field of ExecutionRequestsV1.
+type ConsolidationRequestV1 struct {
+	// sourceAddress: DATA, 20 Bytes
+	SourceAddress hexutil.Bytes `json:"source_address"`
+	// sourcePubkey: DATA, 48 Bytes
+	SourcePubkey hexutil.Bytes `json:"source_pubkey"`
+	// targetPubkey: DATA, 48 Bytes
+	TargetPubkey hexutil.Bytes `json:"target_pubkey"`
+}
+
+func (cr *ConsolidationRequestV1) ToProto() (*v1.ConsolidationRequest, error) {
+	srcAddress, err := bytesutil.DecodeHexWithLength(cr.SourceAddress.String(), common.AddressLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "source_address")
+	}
+	sourcePubkey, err := bytesutil.DecodeHexWithLength(cr.SourcePubkey.String(), fieldparams.BLSPubkeyLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "source_pubkey")
+	}
+	targetPubkey, err := bytesutil.DecodeHexWithLength(cr.TargetPubkey.String(), fieldparams.BLSPubkeyLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "target_pubkey")
+	}
+	return &v1.ConsolidationRequest{
+		SourceAddress: srcAddress,
+		SourcePubkey:  sourcePubkey,
+		TargetPubkey:  targetPubkey,
+	}, nil
+}
+
 // ErrorMessage is a JSON representation of the builder API's returned error message.
 type ErrorMessage struct {
 	Code        int      `json:"code"`
--- a/api/client/builder/types_test.go
+++ b/api/client/builder/types_test.go
@@ -154,6 +154,64 @@ var testExampleHeaderResponseDeneb = `{
  }
 }`

+var testExampleHeaderResponseElectra = `{
+  "version": "electra",
+  "data": {
+    "message": {
+      "header": {
+        "parent_hash": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "fee_recipient": "0xabcf8e0d4e9587369b2301d0790347320302cc09",
+        "state_root": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "receipts_root": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "logs_bloom": "0x00000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000",
+        "prev_randao": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "block_number": "1",
+        "gas_limit": "1",
+        "gas_used": "1",
+        "timestamp": "1",
+        "extra_data": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "base_fee_per_gas": "1",
+        "blob_gas_used": "1",
+        "excess_blob_gas": "1",
+        "block_hash": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "transactions_root": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+        "withdrawals_root": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2"
+      },
+      "blob_kzg_commitments": [
+        "0xa94170080872584e54a1cf092d845703b13907f2e6b3b1c0ad573b910530499e3bcd48c6378846b80d2bfa58c81cf3d5"
+      ],
+      "execution_requests": {
+        "deposits": [
+          {
+            "pubkey": "0x93247f2209abcacf57b75a51dafae777f9dd38bc7053d1af526f220a7489a6d3a2753e5f3e8b1cfe39b56f43611df74a",
+            "withdrawal_credentials": "0xcf8e0d4e9587369b2301d0790347320302cc0943d5a1884560367e8208d920f2",
+            "amount": "1",
+            "signature": "0x1b66ac1fb663c9bc59509846d6ec05345bd908eda73e670af888da41af171505cc411d61252fb6cb3fa0017b679f8bb2305b26a285fa2737f175668d0dff91cc1b66ac1fb663c9bc59509846d6ec05345bd908eda73e670af888da41af171505",
+            "index": "1"
+          }
+        ],
+        "withdrawals": [
+          {
+            "source_address": "0xabcf8e0d4e9587369b2301d0790347320302cc09",
+            "validator_pubkey": "0x93247f2209abcacf57b75a51dafae777f9dd38bc7053d1af526f220a7489a6d3a2753e5f3e8b1cfe39b56f43611df74a",
+            "amount": "1"
+          }
+        ],
+        "consolidations": [
+          {
+            "source_address": "0xabcf8e0d4e9587369b2301d0790347320302cc09",
+            "source_pubkey": "0x93247f2209abcacf57b75a51dafae777f9dd38bc7053d1af526f220a7489a6d3a2753e5f3e8b1cfe39b56f43611df74a",
+            "target_pubkey": "0x93247f2209abcacf57b75a51dafae777f9dd38bc7053d1af526f220a7489a6d3a2753e5f3e8b1cfe39b56f43611df74a"
+          }
+        ]
+      },
+      "value": "652312848583266388373324160190187140051835877600158453279131187530910662656",
+      "pubkey": "0x93247f2209abcacf57b75a51dafae777f9dd38bc7053d1af526f220a7489a6d3a2753e5f3e8b1cfe39b56f43611df74a"
+    },
+    "signature": "0x1b66ac1fb663c9bc59509846d6ec05345bd908eda73e670af888da41af171505cc411d61252fb6cb3fa0017b679f8bb2305b26a285fa2737f175668d0dff91cc1b66ac1fb663c9bc59509846d6ec05345bd908eda73e670af888da41af171505"
+  }
+}`
+
 var testExampleHeaderResponseDenebNoBundle = `{
  "version": "deneb",
  "data": {
@@ -1924,9 +1982,9 @@ func TestEmptyResponseBody(t *testing.T) {
 		emptyResponse := &ExecutionPayloadResponse{}
 		require.NoError(t, json.Unmarshal(empty, emptyResponse))
 		_, err := emptyResponse.ParsePayload()
-		require.ErrorIs(t, err, consensusblocks.ErrUnsupportedVersion)
+		require.ErrorContains(t, "unsupported version", err)
 	})
-	versions := []int{version.Bellatrix, version.Capella, version.Deneb}
+	versions := []int{version.Bellatrix, version.Capella, version.Deneb, version.Electra}
 	for i := range versions {
 		vstr := version.String(versions[i])
 		t.Run("populated version without payload"+vstr, func(t *testing.T) {
--- a/api/grpc/grpcutils.go
+++ b/api/grpc/grpcutils.go
@@ -74,7 +74,7 @@ func AppendHeaders(parent context.Context, headers []string) context.Context {
 				logrus.Warnf("Incorrect gRPC header flag format. Skipping %v", keyValue[0])
 				continue
 			}
-			parent = metadata.AppendToOutgoingContext(parent, keyValue[0], strings.Join(keyValue[1:], "="))
+			parent = metadata.AppendToOutgoingContext(parent, keyValue[0], strings.Join(keyValue[1:], "=")) // nolint:fatcontext
 		}
 	}
 	return parent
--- a/api/server/structs/BUILD.bazel
+++ b/api/server/structs/BUILD.bazel
@@ -28,6 +28,7 @@ go_library(
        "//api/server:go_default_library",
        "//beacon-chain/state:go_default_library",
        "//config/fieldparams:go_default_library",
+        "//config/params:go_default_library",
        "//consensus-types/interfaces:go_default_library",
        "//consensus-types/primitives:go_default_library",
        "//consensus-types/validator:go_default_library",
--- a/api/server/structs/conversions.go
+++ b/api/server/structs/conversions.go
@@ -9,6 +9,7 @@ import (
 	"github.com/pkg/errors"
 	"github.com/prysmaticlabs/prysm/v5/api/server"
 	fieldparams "github.com/prysmaticlabs/prysm/v5/config/fieldparams"
+	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/validator"
 	"github.com/prysmaticlabs/prysm/v5/container/slice"
@@ -51,6 +52,9 @@ func HistoricalSummaryFromConsensus(s *eth.HistoricalSummary) *HistoricalSummary
 }

 func (s *SignedBLSToExecutionChange) ToConsensus() (*eth.SignedBLSToExecutionChange, error) {
+	if s.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
+	}
 	change, err := s.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
@@ -102,14 +106,17 @@ func SignedBLSChangeFromConsensus(ch *eth.SignedBLSToExecutionChange) *SignedBLS

 func SignedBLSChangesToConsensus(src []*SignedBLSToExecutionChange) ([]*eth.SignedBLSToExecutionChange, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "SignedBLSToExecutionChanges")
 	}
 	err := slice.VerifyMaxLength(src, 16)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "SignedBLSToExecutionChanges")
 	}
 	changes := make([]*eth.SignedBLSToExecutionChange, len(src))
 	for i, ch := range src {
+		if ch == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d]", i))
+		}
 		changes[i], err = ch.ToConsensus()
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d]", i))
@@ -155,6 +162,9 @@ func ForkFromConsensus(f *eth.Fork) *Fork {
 }

 func (s *SignedValidatorRegistration) ToConsensus() (*eth.SignedValidatorRegistrationV1, error) {
+	if s.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
+	}
 	msg, err := s.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
@@ -211,6 +221,9 @@ func SignedValidatorRegistrationFromConsensus(vr *eth.SignedValidatorRegistratio
 }

 func (s *SignedContributionAndProof) ToConsensus() (*eth.SignedContributionAndProof, error) {
+	if s.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
+	}
 	msg, err := s.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
@@ -235,6 +248,9 @@ func SignedContributionAndProofFromConsensus(c *eth.SignedContributionAndProof)
 }

 func (c *ContributionAndProof) ToConsensus() (*eth.ContributionAndProof, error) {
+	if c.Contribution == nil {
+		return nil, server.NewDecodeError(errNilValue, "Contribution")
+	}
 	contribution, err := c.Contribution.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Contribution")
@@ -243,7 +259,7 @@ func (c *ContributionAndProof) ToConsensus() (*eth.ContributionAndProof, error)
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AggregatorIndex")
 	}
-	selectionProof, err := bytesutil.DecodeHexWithLength(c.SelectionProof, 96)
+	selectionProof, err := bytesutil.DecodeHexWithLength(c.SelectionProof, fieldparams.BLSSignatureLength)
 	if err != nil {
 		return nil, server.NewDecodeError(err, "SelectionProof")
 	}
@@ -306,6 +322,9 @@ func SyncCommitteeContributionFromConsensus(c *eth.SyncCommitteeContribution) *S
 }

 func (s *SignedAggregateAttestationAndProof) ToConsensus() (*eth.SignedAggregateAttestationAndProof, error) {
+	if s.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
+	}
 	msg, err := s.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
@@ -326,11 +345,14 @@ func (a *AggregateAttestationAndProof) ToConsensus() (*eth.AggregateAttestationA
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AggregatorIndex")
 	}
+	if a.Aggregate == nil {
+		return nil, server.NewDecodeError(errNilValue, "Aggregate")
+	}
 	agg, err := a.Aggregate.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Aggregate")
 	}
-	proof, err := bytesutil.DecodeHexWithLength(a.SelectionProof, 96)
+	proof, err := bytesutil.DecodeHexWithLength(a.SelectionProof, fieldparams.BLSSignatureLength)
 	if err != nil {
 		return nil, server.NewDecodeError(err, "SelectionProof")
 	}
@@ -342,6 +364,9 @@ func (a *AggregateAttestationAndProof) ToConsensus() (*eth.AggregateAttestationA
 }

 func (s *SignedAggregateAttestationAndProofElectra) ToConsensus() (*eth.SignedAggregateAttestationAndProofElectra, error) {
+	if s.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
+	}
 	msg, err := s.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
@@ -362,11 +387,14 @@ func (a *AggregateAttestationAndProofElectra) ToConsensus() (*eth.AggregateAttes
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AggregatorIndex")
 	}
+	if a.Aggregate == nil {
+		return nil, server.NewDecodeError(errNilValue, "Aggregate")
+	}
 	agg, err := a.Aggregate.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Aggregate")
 	}
-	proof, err := bytesutil.DecodeHexWithLength(a.SelectionProof, 96)
+	proof, err := bytesutil.DecodeHexWithLength(a.SelectionProof, fieldparams.BLSSignatureLength)
 	if err != nil {
 		return nil, server.NewDecodeError(err, "SelectionProof")
 	}
@@ -382,6 +410,9 @@ func (a *Attestation) ToConsensus() (*eth.Attestation, error) {
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AggregationBits")
 	}
+	if a.Data == nil {
+		return nil, server.NewDecodeError(errNilValue, "Data")
+	}
 	data, err := a.Data.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Data")
@@ -411,6 +442,9 @@ func (a *AttestationElectra) ToConsensus() (*eth.AttestationElectra, error) {
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AggregationBits")
 	}
+	if a.Data == nil {
+		return nil, server.NewDecodeError(errNilValue, "Data")
+	}
 	data, err := a.Data.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Data")
@@ -432,6 +466,15 @@ func (a *AttestationElectra) ToConsensus() (*eth.AttestationElectra, error) {
 	}, nil
 }

+func SingleAttFromConsensus(a *eth.SingleAttestation) *SingleAttestation {
+	return &SingleAttestation{
+		CommitteeIndex: fmt.Sprintf("%d", a.CommitteeId),
+		AttesterIndex:  fmt.Sprintf("%d", a.AttesterIndex),
+		Data:           AttDataFromConsensus(a.Data),
+		Signature:      hexutil.Encode(a.Signature),
+	}
+}
+
 func (a *SingleAttestation) ToConsensus() (*eth.SingleAttestation, error) {
 	ci, err := strconv.ParseUint(a.CommitteeIndex, 10, 64)
 	if err != nil {
@@ -441,6 +484,9 @@ func (a *SingleAttestation) ToConsensus() (*eth.SingleAttestation, error) {
 	if err != nil {
 		return nil, server.NewDecodeError(err, "AttesterIndex")
 	}
+	if a.Data == nil {
+		return nil, server.NewDecodeError(errNilValue, "Data")
+	}
 	data, err := a.Data.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Data")
@@ -480,10 +526,16 @@ func (a *AttestationData) ToConsensus() (*eth.AttestationData, error) {
 	if err != nil {
 		return nil, server.NewDecodeError(err, "BeaconBlockRoot")
 	}
+	if a.Source == nil {
+		return nil, server.NewDecodeError(errNilValue, "Source")
+	}
 	source, err := a.Source.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Source")
 	}
+	if a.Target == nil {
+		return nil, server.NewDecodeError(errNilValue, "Target")
+	}
 	target, err := a.Target.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Target")
@@ -583,15 +635,17 @@ func (b *BeaconCommitteeSubscription) ToConsensus() (*validator.BeaconCommitteeS
 }

 func (e *SignedVoluntaryExit) ToConsensus() (*eth.SignedVoluntaryExit, error) {
-	sig, err := bytesutil.DecodeHexWithLength(e.Signature, fieldparams.BLSSignatureLength)
-	if err != nil {
-		return nil, server.NewDecodeError(err, "Signature")
+	if e.Message == nil {
+		return nil, server.NewDecodeError(errNilValue, "Message")
 	}
 	exit, err := e.Message.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Message")
 	}
-
+	sig, err := bytesutil.DecodeHexWithLength(e.Signature, fieldparams.BLSSignatureLength)
+	if err != nil {
+		return nil, server.NewDecodeError(err, "Signature")
+	}
 	return &eth.SignedVoluntaryExit{
 		Exit:      exit,
 		Signature: sig,
@@ -694,10 +748,16 @@ func Eth1DataFromConsensus(e1d *eth.Eth1Data) *Eth1Data {
 }

 func (s *ProposerSlashing) ToConsensus() (*eth.ProposerSlashing, error) {
+	if s.SignedHeader1 == nil {
+		return nil, server.NewDecodeError(errNilValue, "SignedHeader1")
+	}
 	h1, err := s.SignedHeader1.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "SignedHeader1")
 	}
+	if s.SignedHeader2 == nil {
+		return nil, server.NewDecodeError(errNilValue, "SignedHeader2")
+	}
 	h2, err := s.SignedHeader2.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "SignedHeader2")
@@ -710,10 +770,16 @@ func (s *ProposerSlashing) ToConsensus() (*eth.ProposerSlashing, error) {
 }

 func (s *AttesterSlashing) ToConsensus() (*eth.AttesterSlashing, error) {
+	if s.Attestation1 == nil {
+		return nil, server.NewDecodeError(errNilValue, "Attestation1")
+	}
 	att1, err := s.Attestation1.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Attestation1")
 	}
+	if s.Attestation2 == nil {
+		return nil, server.NewDecodeError(errNilValue, "Attestation2")
+	}
 	att2, err := s.Attestation2.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Attestation2")
@@ -722,10 +788,16 @@ func (s *AttesterSlashing) ToConsensus() (*eth.AttesterSlashing, error) {
 }

 func (s *AttesterSlashingElectra) ToConsensus() (*eth.AttesterSlashingElectra, error) {
+	if s.Attestation1 == nil {
+		return nil, server.NewDecodeError(errNilValue, "Attestation1")
+	}
 	att1, err := s.Attestation1.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Attestation1")
 	}
+	if s.Attestation2 == nil {
+		return nil, server.NewDecodeError(errNilValue, "Attestation2")
+	}
 	att2, err := s.Attestation2.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Attestation2")
@@ -734,6 +806,10 @@ func (s *AttesterSlashingElectra) ToConsensus() (*eth.AttesterSlashingElectra, e
 }

 func (a *IndexedAttestation) ToConsensus() (*eth.IndexedAttestation, error) {
+	if err := slice.VerifyMaxLength(a.AttestingIndices, params.BeaconConfig().MaxValidatorsPerCommittee); err != nil {
+		return nil, err
+	}
+
 	indices := make([]uint64, len(a.AttestingIndices))
 	var err error
 	for i, ix := range a.AttestingIndices {
@@ -742,6 +818,9 @@ func (a *IndexedAttestation) ToConsensus() (*eth.IndexedAttestation, error) {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("AttestingIndices[%d]", i))
 		}
 	}
+	if a.Data == nil {
+		return nil, server.NewDecodeError(errNilValue, "Data")
+	}
 	data, err := a.Data.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Data")
@@ -759,6 +838,13 @@ func (a *IndexedAttestation) ToConsensus() (*eth.IndexedAttestation, error) {
 }

 func (a *IndexedAttestationElectra) ToConsensus() (*eth.IndexedAttestationElectra, error) {
+	if err := slice.VerifyMaxLength(
+		a.AttestingIndices,
+		params.BeaconConfig().MaxValidatorsPerCommittee*params.BeaconConfig().MaxCommitteesPerSlot,
+	); err != nil {
+		return nil, err
+	}
+
 	indices := make([]uint64, len(a.AttestingIndices))
 	var err error
 	for i, ix := range a.AttestingIndices {
@@ -767,6 +853,9 @@ func (a *IndexedAttestationElectra) ToConsensus() (*eth.IndexedAttestationElectr
 			return nil, server.NewDecodeError(err, fmt.Sprintf("AttestingIndices[%d]", i))
 		}
 	}
+	if a.Data == nil {
+		return nil, server.NewDecodeError(errNilValue, "Data")
+	}
 	data, err := a.Data.ToConsensus()
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Data")
@@ -922,11 +1011,11 @@ func (d *DepositRequest) ToConsensus() (*enginev1.DepositRequest, error) {

 func ProposerSlashingsToConsensus(src []*ProposerSlashing) ([]*eth.ProposerSlashing, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "ProposerSlashings")
 	}
 	err := slice.VerifyMaxLength(src, 16)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "ProposerSlashings")
 	}
 	proposerSlashings := make([]*eth.ProposerSlashing, len(src))
 	for i, s := range src {
@@ -1055,11 +1144,11 @@ func ProposerSlashingFromConsensus(src *eth.ProposerSlashing) *ProposerSlashing

 func AttesterSlashingsToConsensus(src []*AttesterSlashing) ([]*eth.AttesterSlashing, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "AttesterSlashings")
 	}
 	err := slice.VerifyMaxLength(src, 2)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "AttesterSlashings")
 	}

 	attesterSlashings := make([]*eth.AttesterSlashing, len(src))
@@ -1070,10 +1159,19 @@ func AttesterSlashingsToConsensus(src []*AttesterSlashing) ([]*eth.AttesterSlash
 		if s.Attestation1 == nil {
 			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation1", i))
 		}
+
+		if s.Attestation1.Data == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation1.Data", i))
+		}
+
 		if s.Attestation2 == nil {
 			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation2", i))
 		}

+		if s.Attestation2.Data == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation2.Data", i))
+		}
+
 		a1Sig, err := bytesutil.DecodeHexWithLength(s.Attestation1.Signature, fieldparams.BLSSignatureLength)
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation1.Signature", i))
@@ -1090,6 +1188,7 @@ func AttesterSlashingsToConsensus(src []*AttesterSlashing) ([]*eth.AttesterSlash
 			}
 			a1AttestingIndices[j] = attestingIndex
 		}
+
 		a1Data, err := s.Attestation1.Data.ToConsensus()
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation1.Data", i))
@@ -1187,11 +1286,11 @@ func AttesterSlashingFromConsensus(src *eth.AttesterSlashing) *AttesterSlashing

 func AttesterSlashingsElectraToConsensus(src []*AttesterSlashingElectra) ([]*eth.AttesterSlashingElectra, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "AttesterSlashingsElectra")
 	}
-	err := slice.VerifyMaxLength(src, 2)
+	err := slice.VerifyMaxLength(src, fieldparams.MaxAttesterSlashingsElectra)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "AttesterSlashingsElectra")
 	}

 	attesterSlashings := make([]*eth.AttesterSlashingElectra, len(src))
@@ -1199,18 +1298,28 @@ func AttesterSlashingsElectraToConsensus(src []*AttesterSlashingElectra) ([]*eth
 		if s == nil {
 			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d]", i))
 		}
+
 		if s.Attestation1 == nil {
 			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation1", i))
 		}
+
+		if s.Attestation1.Data == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation1.Data", i))
+		}
+
 		if s.Attestation2 == nil {
 			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation2", i))
 		}

+		if s.Attestation2.Data == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d].Attestation2.Data", i))
+		}
+
 		a1Sig, err := bytesutil.DecodeHexWithLength(s.Attestation1.Signature, fieldparams.BLSSignatureLength)
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation1.Signature", i))
 		}
-		err = slice.VerifyMaxLength(s.Attestation1.AttestingIndices, 2048)
+		err = slice.VerifyMaxLength(s.Attestation1.AttestingIndices, params.BeaconConfig().MaxValidatorsPerCommittee*params.BeaconConfig().MaxCommitteesPerSlot)
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation1.AttestingIndices", i))
 		}
@@ -1230,7 +1339,7 @@ func AttesterSlashingsElectraToConsensus(src []*AttesterSlashingElectra) ([]*eth
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation2.Signature", i))
 		}
-		err = slice.VerifyMaxLength(s.Attestation2.AttestingIndices, 2048)
+		err = slice.VerifyMaxLength(s.Attestation2.AttestingIndices, params.BeaconConfig().MaxValidatorsPerCommittee*params.BeaconConfig().MaxCommitteesPerSlot)
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d].Attestation2.AttestingIndices", i))
 		}
@@ -1319,15 +1428,18 @@ func AttesterSlashingElectraFromConsensus(src *eth.AttesterSlashingElectra) *Att

 func AttsToConsensus(src []*Attestation) ([]*eth.Attestation, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "Attestations")
 	}
 	err := slice.VerifyMaxLength(src, 128)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "Attestations")
 	}

 	atts := make([]*eth.Attestation, len(src))
 	for i, a := range src {
+		if a == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d]", i))
+		}
 		atts[i], err = a.ToConsensus()
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d]", i))
@@ -1346,15 +1458,18 @@ func AttsFromConsensus(src []*eth.Attestation) []*Attestation {

 func AttsElectraToConsensus(src []*AttestationElectra) ([]*eth.AttestationElectra, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "AttestationsElectra")
 	}
 	err := slice.VerifyMaxLength(src, 8)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "AttestationsElectra")
 	}

 	atts := make([]*eth.AttestationElectra, len(src))
 	for i, a := range src {
+		if a == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d]", i))
+		}
 		atts[i], err = a.ToConsensus()
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d]", i))
@@ -1373,11 +1488,11 @@ func AttsElectraFromConsensus(src []*eth.AttestationElectra) []*AttestationElect

 func DepositsToConsensus(src []*Deposit) ([]*eth.Deposit, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "Deposits")
 	}
 	err := slice.VerifyMaxLength(src, 16)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "Deposits")
 	}

 	deposits := make([]*eth.Deposit, len(src))
@@ -1449,15 +1564,18 @@ func DepositsFromConsensus(src []*eth.Deposit) []*Deposit {

 func SignedExitsToConsensus(src []*SignedVoluntaryExit) ([]*eth.SignedVoluntaryExit, error) {
 	if src == nil {
-		return nil, errNilValue
+		return nil, server.NewDecodeError(errNilValue, "SignedVoluntaryExits")
 	}
 	err := slice.VerifyMaxLength(src, 16)
 	if err != nil {
-		return nil, err
+		return nil, server.NewDecodeError(err, "SignedVoluntaryExits")
 	}

 	exits := make([]*eth.SignedVoluntaryExit, len(src))
 	for i, e := range src {
+		if e == nil {
+			return nil, server.NewDecodeError(errNilValue, fmt.Sprintf("[%d]", i))
+		}
 		exits[i], err = e.ToConsensus()
 		if err != nil {
 			return nil, server.NewDecodeError(err, fmt.Sprintf("[%d]", i))
--- a/api/server/structs/conversions_block.go
+++ b/api/server/structs/conversions_block.go
@@ -9,6 +9,7 @@ import (
 	"github.com/pkg/errors"
 	"github.com/prysmaticlabs/prysm/v5/api/server"
 	fieldparams "github.com/prysmaticlabs/prysm/v5/config/fieldparams"
+	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/interfaces"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/container/slice"
@@ -2519,6 +2520,7 @@ func (b *BeaconBlockContentsElectra) ToConsensus() (*eth.BeaconBlockContentsElec
 	}, nil
 }

+// nolint:gocognit
 func (b *BeaconBlockElectra) ToConsensus() (*eth.BeaconBlockElectra, error) {
 	if b == nil {
 		return nil, errNilValue
@@ -2706,6 +2708,9 @@ func (b *BeaconBlockElectra) ToConsensus() (*eth.BeaconBlockElectra, error) {
 		return nil, server.NewDecodeError(errors.New("nil execution requests"), "Body.ExequtionRequests")
 	}

+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Deposits, params.BeaconConfig().MaxDepositRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	depositRequests := make([]*enginev1.DepositRequest, len(b.Body.ExecutionRequests.Deposits))
 	for i, d := range b.Body.ExecutionRequests.Deposits {
 		depositRequests[i], err = d.ToConsensus()
@@ -2714,6 +2719,9 @@ func (b *BeaconBlockElectra) ToConsensus() (*eth.BeaconBlockElectra, error) {
 		}
 	}

+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Withdrawals, params.BeaconConfig().MaxWithdrawalRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	withdrawalRequests := make([]*enginev1.WithdrawalRequest, len(b.Body.ExecutionRequests.Withdrawals))
 	for i, w := range b.Body.ExecutionRequests.Withdrawals {
 		withdrawalRequests[i], err = w.ToConsensus()
@@ -2722,6 +2730,9 @@ func (b *BeaconBlockElectra) ToConsensus() (*eth.BeaconBlockElectra, error) {
 		}
 	}

+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Consolidations, params.BeaconConfig().MaxConsolidationsRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	consolidationRequests := make([]*enginev1.ConsolidationRequest, len(b.Body.ExecutionRequests.Consolidations))
 	for i, c := range b.Body.ExecutionRequests.Consolidations {
 		consolidationRequests[i], err = c.ToConsensus()
@@ -3003,9 +3014,14 @@ func (b *BlindedBeaconBlockElectra) ToConsensus() (*eth.BlindedBeaconBlockElectr
 	if err != nil {
 		return nil, server.NewDecodeError(err, "Body.ExecutionPayload.ExcessBlobGas")
 	}
+
 	if b.Body.ExecutionRequests == nil {
 		return nil, server.NewDecodeError(errors.New("nil execution requests"), "Body.ExecutionRequests")
 	}
+
+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Deposits, params.BeaconConfig().MaxDepositRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	depositRequests := make([]*enginev1.DepositRequest, len(b.Body.ExecutionRequests.Deposits))
 	for i, d := range b.Body.ExecutionRequests.Deposits {
 		depositRequests[i], err = d.ToConsensus()
@@ -3014,6 +3030,9 @@ func (b *BlindedBeaconBlockElectra) ToConsensus() (*eth.BlindedBeaconBlockElectr
 		}
 	}

+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Withdrawals, params.BeaconConfig().MaxWithdrawalRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	withdrawalRequests := make([]*enginev1.WithdrawalRequest, len(b.Body.ExecutionRequests.Withdrawals))
 	for i, w := range b.Body.ExecutionRequests.Withdrawals {
 		withdrawalRequests[i], err = w.ToConsensus()
@@ -3022,6 +3041,9 @@ func (b *BlindedBeaconBlockElectra) ToConsensus() (*eth.BlindedBeaconBlockElectr
 		}
 	}

+	if err = slice.VerifyMaxLength(b.Body.ExecutionRequests.Consolidations, params.BeaconConfig().MaxConsolidationsRequestsPerPayload); err != nil {
+		return nil, err
+	}
 	consolidationRequests := make([]*enginev1.ConsolidationRequest, len(b.Body.ExecutionRequests.Consolidations))
 	for i, c := range b.Body.ExecutionRequests.Consolidations {
 		consolidationRequests[i], err = c.ToConsensus()
--- a/api/server/structs/conversions_test.go
+++ b/api/server/structs/conversions_test.go
@@ -24,3 +24,96 @@ func TestDepositSnapshotFromConsensus(t *testing.T) {
 	require.Equal(t, "0x1234", res.ExecutionBlockHash)
 	require.Equal(t, "67890", res.ExecutionBlockHeight)
 }
+
+func TestSignedBLSToExecutionChange_ToConsensus(t *testing.T) {
+	s := &SignedBLSToExecutionChange{Message: nil, Signature: ""}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestSignedValidatorRegistration_ToConsensus(t *testing.T) {
+	s := &SignedValidatorRegistration{Message: nil, Signature: ""}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestSignedContributionAndProof_ToConsensus(t *testing.T) {
+	s := &SignedContributionAndProof{Message: nil, Signature: ""}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestContributionAndProof_ToConsensus(t *testing.T) {
+	c := &ContributionAndProof{
+		Contribution:    nil,
+		AggregatorIndex: "invalid",
+		SelectionProof:  "",
+	}
+	_, err := c.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestSignedAggregateAttestationAndProof_ToConsensus(t *testing.T) {
+	s := &SignedAggregateAttestationAndProof{Message: nil, Signature: ""}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestAggregateAttestationAndProof_ToConsensus(t *testing.T) {
+	a := &AggregateAttestationAndProof{
+		AggregatorIndex: "1",
+		Aggregate:       nil,
+		SelectionProof:  "",
+	}
+	_, err := a.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestAttestation_ToConsensus(t *testing.T) {
+	a := &Attestation{
+		AggregationBits: "0x10",
+		Data:            nil,
+		Signature:       "",
+	}
+	_, err := a.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestSingleAttestation_ToConsensus(t *testing.T) {
+	s := &SingleAttestation{
+		CommitteeIndex: "1",
+		AttesterIndex:  "1",
+		Data:           nil,
+		Signature:      "",
+	}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestSignedVoluntaryExit_ToConsensus(t *testing.T) {
+	s := &SignedVoluntaryExit{Message: nil, Signature: ""}
+	_, err := s.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestProposerSlashing_ToConsensus(t *testing.T) {
+	p := &ProposerSlashing{SignedHeader1: nil, SignedHeader2: nil}
+	_, err := p.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestAttesterSlashing_ToConsensus(t *testing.T) {
+	a := &AttesterSlashing{Attestation1: nil, Attestation2: nil}
+	_, err := a.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
+
+func TestIndexedAttestation_ToConsensus(t *testing.T) {
+	a := &IndexedAttestation{
+		AttestingIndices: []string{"1"},
+		Data:             nil,
+		Signature:        "invalid",
+	}
+	_, err := a.ToConsensus()
+	require.ErrorContains(t, errNilValue.Error(), err)
+}
--- a/beacon-chain/blockchain/BUILD.bazel
+++ b/beacon-chain/blockchain/BUILD.bazel
@@ -43,6 +43,7 @@ go_library(
        "//beacon-chain/cache:go_default_library",
        "//beacon-chain/core/altair:go_default_library",
        "//beacon-chain/core/blocks:go_default_library",
+        "//beacon-chain/core/electra:go_default_library",
        "//beacon-chain/core/epoch/precompute:go_default_library",
        "//beacon-chain/core/feed:go_default_library",
        "//beacon-chain/core/feed/state:go_default_library",
--- a/beacon-chain/blockchain/blockchain_test.go
+++ b/beacon-chain/blockchain/blockchain_test.go
@@ -2,6 +2,7 @@ package blockchain

 import (
 	"io"
+	"os"
 	"testing"

 	"github.com/sirupsen/logrus"
@@ -11,5 +12,5 @@ func TestMain(m *testing.M) {
 	logrus.SetLevel(logrus.DebugLevel)
 	logrus.SetOutput(io.Discard)

-	m.Run()
+	os.Exit(m.Run())
 }
--- a/beacon-chain/blockchain/execution_engine.go
+++ b/beacon-chain/blockchain/execution_engine.go
@@ -268,6 +268,9 @@ func (s *Service) notifyNewPayload(ctx context.Context, preStateVersion int,
 		if err != nil {
 			return false, errors.Wrap(err, "could not get execution requests")
 		}
+		if requests == nil {
+			return false, errors.New("nil execution requests")
+		}
 	}
 	lastValidHash, err = s.cfg.ExecutionEngineCaller.NewPayload(ctx, payload, versionedHashes, parentRoot, requests)

--- a/beacon-chain/blockchain/process_block.go
+++ b/beacon-chain/blockchain/process_block.go
@@ -512,17 +512,11 @@ func missingIndices(bs *filesystem.BlobStorage, root [32]byte, expected [][]byte
 	if len(expected) > maxBlobsPerBlock {
 		return nil, errMaxBlobsExceeded
 	}
-	indices, err := bs.Indices(root, slot)
-	if err != nil {
-		return nil, err
-	}
+	indices := bs.Summary(root)
 	missing := make(map[uint64]struct{}, len(expected))
 	for i := range expected {
-		ui := uint64(i)
-		if len(expected[i]) > 0 {
-			if !indices[i] {
-				missing[ui] = struct{}{}
-			}
+		if len(expected[i]) > 0 && !indices.HasIndex(uint64(i)) {
+			missing[uint64(i)] = struct{}{}
 		}
 	}
 	return missing, nil
--- a/beacon-chain/blockchain/process_block_helpers.go
+++ b/beacon-chain/blockchain/process_block_helpers.go
@@ -7,6 +7,7 @@ import (
 	"strings"
 	"time"

+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
 	lightclient "github.com/prysmaticlabs/prysm/v5/beacon-chain/core/light-client"

 	"github.com/ethereum/go-ethereum/common"
@@ -552,7 +553,8 @@ func (s *Service) fillInForkChoiceMissingBlocks(ctx context.Context, signed inte

 // inserts finalized deposits into our finalized deposit trie, needs to be
 // called in the background
-func (s *Service) insertFinalizedDeposits(ctx context.Context, fRoot [32]byte) {
+// Post-Electra: prunes all proofs and pending deposits in the cache
+func (s *Service) insertFinalizedDepositsAndPrune(ctx context.Context, fRoot [32]byte) {
 	ctx, span := trace.StartSpan(ctx, "blockChain.insertFinalizedDeposits")
 	defer span.End()
 	startTime := time.Now()
@@ -563,6 +565,16 @@ func (s *Service) insertFinalizedDeposits(ctx context.Context, fRoot [32]byte) {
 		log.WithError(err).Error("could not fetch finalized state")
 		return
 	}
+
+	// Check if we should prune all pending deposits.
+	// In post-Electra(after the legacy deposit mechanism is deprecated),
+	// we can prune all pending deposits in the deposit cache.
+	// See: https://eips.ethereum.org/EIPS/eip-6110#eth1data-poll-deprecation
+	if helpers.DepositRequestsStarted(finalizedState) {
+		s.pruneAllPendingDepositsAndProofs(ctx)
+		return
+	}
+
 	// We update the cache up to the last deposit index in the finalized block's state.
 	// We can be confident that these deposits will be included in some block
 	// because the Eth1 follow distance makes such long-range reorgs extremely unlikely.
@@ -591,6 +603,12 @@ func (s *Service) insertFinalizedDeposits(ctx context.Context, fRoot [32]byte) {
 	log.WithField("duration", time.Since(startTime).String()).Debugf("Finalized deposit insertion completed at index %d", finalizedEth1DepIdx)
 }

+// pruneAllPendingDepositsAndProofs prunes all proofs and pending deposits in the cache.
+func (s *Service) pruneAllPendingDepositsAndProofs(ctx context.Context) {
+	s.cfg.DepositCache.PruneAllPendingDeposits(ctx)
+	s.cfg.DepositCache.PruneAllProofs(ctx)
+}
+
 // This ensures that the input root defaults to using genesis root instead of zero hashes. This is needed for handling
 // fork choice justification routine.
 func (s *Service) ensureRootNotZeros(root [32]byte) [32]byte {
--- a/beacon-chain/blockchain/process_block_test.go
+++ b/beacon-chain/blockchain/process_block_test.go
@@ -723,7 +723,7 @@ func TestInsertFinalizedDeposits(t *testing.T) {
 			Signature:             zeroSig[:],
 		}, Proof: [][]byte{root}}, 100+i, int64(i), bytesutil.ToBytes32(root)))
 	}
-	service.insertFinalizedDeposits(ctx, [32]byte{'m', 'o', 'c', 'k'})
+	service.insertFinalizedDepositsAndPrune(ctx, [32]byte{'m', 'o', 'c', 'k'})
 	fDeposits, err := depositCache.FinalizedDeposits(ctx)
 	require.NoError(t, err)
 	assert.Equal(t, 7, int(fDeposits.MerkleTrieIndex()), "Finalized deposits not inserted correctly")
@@ -759,7 +759,7 @@ func TestInsertFinalizedDeposits_PrunePendingDeposits(t *testing.T) {
 			Signature:             zeroSig[:],
 		}, Proof: [][]byte{root}}, 100+i, int64(i), bytesutil.ToBytes32(root))
 	}
-	service.insertFinalizedDeposits(ctx, [32]byte{'m', 'o', 'c', 'k'})
+	service.insertFinalizedDepositsAndPrune(ctx, [32]byte{'m', 'o', 'c', 'k'})
 	fDeposits, err := depositCache.FinalizedDeposits(ctx)
 	require.NoError(t, err)
 	assert.Equal(t, 7, int(fDeposits.MerkleTrieIndex()), "Finalized deposits not inserted correctly")
@@ -799,7 +799,7 @@ func TestInsertFinalizedDeposits_MultipleFinalizedRoutines(t *testing.T) {
 	}
 	// Insert 3 deposits before hand.
 	require.NoError(t, depositCache.InsertFinalizedDeposits(ctx, 2, [32]byte{}, 0))
-	service.insertFinalizedDeposits(ctx, [32]byte{'m', 'o', 'c', 'k'})
+	service.insertFinalizedDepositsAndPrune(ctx, [32]byte{'m', 'o', 'c', 'k'})
 	fDeposits, err := depositCache.FinalizedDeposits(ctx)
 	require.NoError(t, err)
 	assert.Equal(t, 5, int(fDeposits.MerkleTrieIndex()), "Finalized deposits not inserted correctly")
@@ -810,7 +810,7 @@ func TestInsertFinalizedDeposits_MultipleFinalizedRoutines(t *testing.T) {
 	}

 	// Insert New Finalized State with higher deposit count.
-	service.insertFinalizedDeposits(ctx, [32]byte{'m', 'o', 'c', 'k', '2'})
+	service.insertFinalizedDepositsAndPrune(ctx, [32]byte{'m', 'o', 'c', 'k', '2'})
 	fDeposits, err = depositCache.FinalizedDeposits(ctx)
 	require.NoError(t, err)
 	assert.Equal(t, 12, int(fDeposits.MerkleTrieIndex()), "Finalized deposits not inserted correctly")
@@ -1076,6 +1076,48 @@ func TestService_insertSlashingsToForkChoiceStore(t *testing.T) {
 	service.InsertSlashingsToForkChoiceStore(ctx, wb.Block().Body().AttesterSlashings())
 }

+func TestService_insertSlashingsToForkChoiceStoreElectra(t *testing.T) {
+	service, tr := minimalTestService(t)
+	ctx := tr.ctx
+
+	beaconState, privKeys := util.DeterministicGenesisStateElectra(t, 100)
+	att1 := util.HydrateIndexedAttestationElectra(&ethpb.IndexedAttestationElectra{
+		Data: &ethpb.AttestationData{
+			Source: &ethpb.Checkpoint{Epoch: 1},
+		},
+		AttestingIndices: []uint64{0, 1},
+	})
+	domain, err := signing.Domain(beaconState.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, beaconState.GenesisValidatorsRoot())
+	require.NoError(t, err)
+	signingRoot, err := signing.ComputeSigningRoot(att1.Data, domain)
+	assert.NoError(t, err, "Could not get signing root of beacon block header")
+	sig0 := privKeys[0].Sign(signingRoot[:])
+	sig1 := privKeys[1].Sign(signingRoot[:])
+	aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})
+	att1.Signature = aggregateSig.Marshal()
+
+	att2 := util.HydrateIndexedAttestationElectra(&ethpb.IndexedAttestationElectra{
+		AttestingIndices: []uint64{0, 1},
+	})
+	signingRoot, err = signing.ComputeSigningRoot(att2.Data, domain)
+	assert.NoError(t, err, "Could not get signing root of beacon block header")
+	sig0 = privKeys[0].Sign(signingRoot[:])
+	sig1 = privKeys[1].Sign(signingRoot[:])
+	aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
+	att2.Signature = aggregateSig.Marshal()
+	slashings := []*ethpb.AttesterSlashingElectra{
+		{
+			Attestation_1: att1,
+			Attestation_2: att2,
+		},
+	}
+	b := util.NewBeaconBlockElectra()
+	b.Block.Body.AttesterSlashings = slashings
+	wb, err := consensusblocks.NewSignedBeaconBlock(b)
+	require.NoError(t, err)
+	service.InsertSlashingsToForkChoiceStore(ctx, wb.Block().Body().AttesterSlashings())
+}
+
 func TestOnBlock_ProcessBlocksParallel(t *testing.T) {
 	service, tr := minimalTestService(t)
 	ctx := tr.ctx
@@ -2255,7 +2297,7 @@ func TestMissingIndices(t *testing.T) {
 	for _, c := range cases {
 		bm, bs := filesystem.NewEphemeralBlobStorageWithMocker(t)
 		t.Run(c.name, func(t *testing.T) {
-			require.NoError(t, bm.CreateFakeIndices(c.root, c.present...))
+			require.NoError(t, bm.CreateFakeIndices(c.root, 0, c.present...))
 			missing, err := missingIndices(bs, c.root, c.expected, 0)
 			if c.err != nil {
 				require.ErrorIs(t, err, c.err)
--- a/beacon-chain/blockchain/receive_block.go
+++ b/beacon-chain/blockchain/receive_block.go
@@ -7,6 +7,7 @@ import (
 	"time"

 	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/electra"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/feed"
 	statefeed "github.com/prysmaticlabs/prysm/v5/beacon-chain/core/feed/state"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
@@ -278,9 +279,10 @@ func (s *Service) executePostFinalizationTasks(ctx context.Context, finalizedSta
 	go func() {
 		s.sendNewFinalizedEvent(ctx, finalizedState)
 	}()
+
 	depCtx, cancel := context.WithTimeout(context.Background(), depositDeadline)
 	go func() {
-		s.insertFinalizedDeposits(depCtx, finalized.Root)
+		s.insertFinalizedDepositsAndPrune(depCtx, finalized.Root)
 		cancel()
 	}()
 }
@@ -468,6 +470,9 @@ func (s *Service) validateStateTransition(ctx context.Context, preState state.Be
 	stateTransitionStartTime := time.Now()
 	postState, err := transition.ExecuteStateTransition(ctx, preState, signed)
 	if err != nil {
+		if ctx.Err() != nil || electra.IsExecutionRequestError(err) {
+			return nil, err
+		}
 		return nil, invalidBlock{error: err}
 	}
 	stateTransitionProcessingTime.Observe(float64(time.Since(stateTransitionStartTime).Milliseconds()))
--- a/beacon-chain/blockchain/receive_block_test.go
+++ b/beacon-chain/blockchain/receive_block_test.go
@@ -455,41 +455,81 @@ func Test_executePostFinalizationTasks(t *testing.T) {
 		Root:  headRoot[:],
 	}))
 	require.NoError(t, headState.SetGenesisValidatorsRoot(params.BeaconConfig().ZeroHash[:]))
+	t.Run("pre deposit request", func(t *testing.T) {
+		require.NoError(t, headState.SetEth1DepositIndex(1))
+		s, tr := minimalTestService(t, WithFinalizedStateAtStartUp(headState))
+		ctx, beaconDB, stateGen := tr.ctx, tr.db, tr.sg

-	s, tr := minimalTestService(t, WithFinalizedStateAtStartUp(headState))
-	ctx, beaconDB, stateGen := tr.ctx, tr.db, tr.sg
+		require.NoError(t, beaconDB.SaveGenesisBlockRoot(ctx, genesisRoot))
+		util.SaveBlock(t, ctx, beaconDB, genesis)
+		require.NoError(t, beaconDB.SaveState(ctx, headState, headRoot))
+		require.NoError(t, beaconDB.SaveState(ctx, headState, genesisRoot))
+		util.SaveBlock(t, ctx, beaconDB, headBlock)
+		require.NoError(t, beaconDB.SaveFinalizedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))

-	require.NoError(t, beaconDB.SaveGenesisBlockRoot(ctx, genesisRoot))
-	util.SaveBlock(t, ctx, beaconDB, genesis)
-	require.NoError(t, beaconDB.SaveState(ctx, headState, headRoot))
-	require.NoError(t, beaconDB.SaveState(ctx, headState, genesisRoot))
-	util.SaveBlock(t, ctx, beaconDB, headBlock)
-	require.NoError(t, beaconDB.SaveFinalizedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))
+		require.NoError(t, err)
+		require.NoError(t, stateGen.SaveState(ctx, headRoot, headState))
+		require.NoError(t, beaconDB.SaveLastValidatedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))

-	require.NoError(t, err)
-	require.NoError(t, stateGen.SaveState(ctx, headRoot, headState))
-	require.NoError(t, beaconDB.SaveLastValidatedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))
+		notifier := &blockchainTesting.MockStateNotifier{RecordEvents: true}
+		s.cfg.StateNotifier = notifier
+		s.executePostFinalizationTasks(s.ctx, headState)

-	notifier := &blockchainTesting.MockStateNotifier{RecordEvents: true}
-	s.cfg.StateNotifier = notifier
-	s.executePostFinalizationTasks(s.ctx, headState)
+		time.Sleep(1 * time.Second) // sleep for a second because event is in a separate go routine
+		require.Equal(t, 1, len(notifier.ReceivedEvents()))
+		e := notifier.ReceivedEvents()[0]
+		assert.Equal(t, statefeed.FinalizedCheckpoint, int(e.Type))
+		fc, ok := e.Data.(*ethpbv1.EventFinalizedCheckpoint)
+		require.Equal(t, true, ok, "event has wrong data type")
+		assert.Equal(t, primitives.Epoch(123), fc.Epoch)
+		assert.DeepEqual(t, headRoot[:], fc.Block)
+		assert.DeepEqual(t, finalizedStRoot[:], fc.State)
+		assert.Equal(t, false, fc.ExecutionOptimistic)

-	time.Sleep(1 * time.Second) // sleep for a second because event is in a separate go routine
-	require.Equal(t, 1, len(notifier.ReceivedEvents()))
-	e := notifier.ReceivedEvents()[0]
-	assert.Equal(t, statefeed.FinalizedCheckpoint, int(e.Type))
-	fc, ok := e.Data.(*ethpbv1.EventFinalizedCheckpoint)
-	require.Equal(t, true, ok, "event has wrong data type")
-	assert.Equal(t, primitives.Epoch(123), fc.Epoch)
-	assert.DeepEqual(t, headRoot[:], fc.Block)
-	assert.DeepEqual(t, finalizedStRoot[:], fc.State)
-	assert.Equal(t, false, fc.ExecutionOptimistic)
+		// check the cache
+		index, ok := headState.ValidatorIndexByPubkey(bytesutil.ToBytes48(key))
+		require.Equal(t, true, ok)
+		require.Equal(t, primitives.ValidatorIndex(0), index) // first index

-	// check the cache
-	index, ok := headState.ValidatorIndexByPubkey(bytesutil.ToBytes48(key))
-	require.Equal(t, true, ok)
-	require.Equal(t, primitives.ValidatorIndex(0), index) // first index
+		// check deposit
+		require.LogsContain(t, logHook, "Finalized deposit insertion completed at index")
+	})
+	t.Run("deposit requests started", func(t *testing.T) {
+		require.NoError(t, headState.SetEth1DepositIndex(1))
+		require.NoError(t, headState.SetDepositRequestsStartIndex(1))
+		s, tr := minimalTestService(t, WithFinalizedStateAtStartUp(headState))
+		ctx, beaconDB, stateGen := tr.ctx, tr.db, tr.sg
+
+		require.NoError(t, beaconDB.SaveGenesisBlockRoot(ctx, genesisRoot))
+		util.SaveBlock(t, ctx, beaconDB, genesis)
+		require.NoError(t, beaconDB.SaveState(ctx, headState, headRoot))
+		require.NoError(t, beaconDB.SaveState(ctx, headState, genesisRoot))
+		util.SaveBlock(t, ctx, beaconDB, headBlock)
+		require.NoError(t, beaconDB.SaveFinalizedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))
+
+		require.NoError(t, err)
+		require.NoError(t, stateGen.SaveState(ctx, headRoot, headState))
+		require.NoError(t, beaconDB.SaveLastValidatedCheckpoint(ctx, &ethpb.Checkpoint{Epoch: slots.ToEpoch(finalizedSlot), Root: headRoot[:]}))
+
+		notifier := &blockchainTesting.MockStateNotifier{RecordEvents: true}
+		s.cfg.StateNotifier = notifier
+		s.executePostFinalizationTasks(s.ctx, headState)
+
+		time.Sleep(1 * time.Second) // sleep for a second because event is in a separate go routine
+		require.Equal(t, 1, len(notifier.ReceivedEvents()))
+		e := notifier.ReceivedEvents()[0]
+		assert.Equal(t, statefeed.FinalizedCheckpoint, int(e.Type))
+		fc, ok := e.Data.(*ethpbv1.EventFinalizedCheckpoint)
+		require.Equal(t, true, ok, "event has wrong data type")
+		assert.Equal(t, primitives.Epoch(123), fc.Epoch)
+		assert.DeepEqual(t, headRoot[:], fc.Block)
+		assert.DeepEqual(t, finalizedStRoot[:], fc.State)
+		assert.Equal(t, false, fc.ExecutionOptimistic)
+
+		// check the cache
+		index, ok := headState.ValidatorIndexByPubkey(bytesutil.ToBytes48(key))
+		require.Equal(t, true, ok)
+		require.Equal(t, primitives.ValidatorIndex(0), index) // first index
+	})

-	// check deposit
-	require.LogsContain(t, logHook, "Finalized deposit insertion completed at index")
 }
--- a/beacon-chain/builder/testing/mock.go
+++ b/beacon-chain/builder/testing/mock.go
@@ -33,6 +33,7 @@ type MockBuilderService struct {
 	Bid                   *ethpb.SignedBuilderBid
 	BidCapella            *ethpb.SignedBuilderBidCapella
 	BidDeneb              *ethpb.SignedBuilderBidDeneb
+	BidElectra            *ethpb.SignedBuilderBidElectra
 	RegistrationCache     *cache.RegistrationCache
 	ErrGetHeader          error
 	ErrRegisterValidator  error
@@ -59,7 +60,7 @@ func (s *MockBuilderService) SubmitBlindedBlock(_ context.Context, b interfaces.
 			return nil, nil, errors.Wrap(err, "could not wrap capella payload")
 		}
 		return w, nil, s.ErrSubmitBlindedBlock
-	case version.Deneb:
+	case version.Deneb, version.Electra:
 		w, err := blocks.WrappedExecutionPayloadDeneb(s.PayloadDeneb)
 		if err != nil {
 			return nil, nil, errors.Wrap(err, "could not wrap deneb payload")
@@ -72,6 +73,9 @@ func (s *MockBuilderService) SubmitBlindedBlock(_ context.Context, b interfaces.

 // GetHeader for mocking.
 func (s *MockBuilderService) GetHeader(_ context.Context, slot primitives.Slot, _ [32]byte, _ [48]byte) (builder.SignedBid, error) {
+	if slots.ToEpoch(slot) >= params.BeaconConfig().ElectraForkEpoch || s.BidElectra != nil {
+		return builder.WrappedSignedBuilderBidElectra(s.BidElectra)
+	}
 	if slots.ToEpoch(slot) >= params.BeaconConfig().DenebForkEpoch || s.BidDeneb != nil {
 		return builder.WrappedSignedBuilderBidDeneb(s.BidDeneb)
 	}
--- a/beacon-chain/cache/cache_test.go
+++ b/beacon-chain/cache/cache_test.go
@@ -1,9 +1,10 @@
 package cache

 import (
+	"os"
 	"testing"
 )

 func TestMain(m *testing.M) {
-	m.Run()
+	os.Exit(m.Run())
 }
--- a/beacon-chain/cache/depositsnapshot/BUILD.bazel
+++ b/beacon-chain/cache/depositsnapshot/BUILD.bazel
@@ -5,6 +5,7 @@ go_library(
    srcs = [
        "deposit_fetcher.go",
        "deposit_inserter.go",
+        "deposit_pruner.go",
        "deposit_tree.go",
        "deposit_tree_snapshot.go",
        "merkle_tree.go",
@@ -35,6 +36,7 @@ go_test(
    srcs = [
        "deposit_cache_test.go",
        "deposit_fetcher_test.go",
+        "deposit_pruner_test.go",
        "deposit_tree_snapshot_test.go",
        "merkle_tree_test.go",
        "spec_test.go",
--- a/beacon-chain/cache/depositsnapshot/deposit_cache_test.go
+++ b/beacon-chain/cache/depositsnapshot/deposit_cache_test.go
@@ -903,189 +903,6 @@ func TestMin(t *testing.T) {

 }

-func TestPruneProofs_Ok(t *testing.T) {
-	dc, err := New()
-	require.NoError(t, err)
-
-	deposits := []struct {
-		blkNum  uint64
-		deposit *ethpb.Deposit
-		index   int64
-	}{
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
-			index: 0,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
-			index: 1,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
-			index: 2,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
-			index: 3,
-		},
-	}
-
-	for _, ins := range deposits {
-		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
-	}
-
-	require.NoError(t, dc.PruneProofs(context.Background(), 1))
-
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
-	assert.NotNil(t, dc.deposits[2].Deposit.Proof)
-	assert.NotNil(t, dc.deposits[3].Deposit.Proof)
-}
-
-func TestPruneProofs_SomeAlreadyPruned(t *testing.T) {
-	dc, err := New()
-	require.NoError(t, err)
-
-	deposits := []struct {
-		blkNum  uint64
-		deposit *ethpb.Deposit
-		index   int64
-	}{
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: nil, Data: &ethpb.Deposit_Data{
-				PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
-			index: 0,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: nil, Data: &ethpb.Deposit_Data{
-				PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}}, index: 1,
-		},
-		{
-			blkNum:  0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(), Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
-			index:   2,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
-			index: 3,
-		},
-	}
-
-	for _, ins := range deposits {
-		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
-	}
-
-	require.NoError(t, dc.PruneProofs(context.Background(), 2))
-
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
-}
-
-func TestPruneProofs_PruneAllWhenDepositIndexTooBig(t *testing.T) {
-	dc, err := New()
-	require.NoError(t, err)
-
-	deposits := []struct {
-		blkNum  uint64
-		deposit *ethpb.Deposit
-		index   int64
-	}{
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
-			index: 0,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
-			index: 1,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
-			index: 2,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
-			index: 3,
-		},
-	}
-
-	for _, ins := range deposits {
-		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
-	}
-
-	require.NoError(t, dc.PruneProofs(context.Background(), 99))
-
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[3].Deposit.Proof)
-}
-
-func TestPruneProofs_CorrectlyHandleLastIndex(t *testing.T) {
-	dc, err := New()
-	require.NoError(t, err)
-
-	deposits := []struct {
-		blkNum  uint64
-		deposit *ethpb.Deposit
-		index   int64
-	}{
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
-			index: 0,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
-			index: 1,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
-			index: 2,
-		},
-		{
-			blkNum: 0,
-			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
-				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
-			index: 3,
-		},
-	}
-
-	for _, ins := range deposits {
-		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
-	}
-
-	require.NoError(t, dc.PruneProofs(context.Background(), 4))
-
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
-	assert.DeepEqual(t, [][]byte(nil), dc.deposits[3].Deposit.Proof)
-}
-
 func TestDepositMap_WorksCorrectly(t *testing.T) {
 	dc, err := New()
 	require.NoError(t, err)
--- a/beacon-chain/cache/depositsnapshot/deposit_fetcher.go
+++ b/beacon-chain/cache/depositsnapshot/deposit_fetcher.go
@@ -178,52 +178,6 @@ func (c *Cache) NonFinalizedDeposits(ctx context.Context, lastFinalizedIndex int
 	return deposits
 }

-// PruneProofs removes proofs from all deposits whose index is equal or less than untilDepositIndex.
-func (c *Cache) PruneProofs(ctx context.Context, untilDepositIndex int64) error {
-	_, span := trace.StartSpan(ctx, "Cache.PruneProofs")
-	defer span.End()
-	c.depositsLock.Lock()
-	defer c.depositsLock.Unlock()
-
-	if untilDepositIndex >= int64(len(c.deposits)) {
-		untilDepositIndex = int64(len(c.deposits) - 1)
-	}
-
-	for i := untilDepositIndex; i >= 0; i-- {
-		// Finding a nil proof means that all proofs up to this deposit have been already pruned.
-		if c.deposits[i].Deposit.Proof == nil {
-			break
-		}
-		c.deposits[i].Deposit.Proof = nil
-	}
-
-	return nil
-}
-
-// PrunePendingDeposits removes any deposit which is older than the given deposit merkle tree index.
-func (c *Cache) PrunePendingDeposits(ctx context.Context, merkleTreeIndex int64) {
-	_, span := trace.StartSpan(ctx, "Cache.PrunePendingDeposits")
-	defer span.End()
-
-	if merkleTreeIndex == 0 {
-		log.Debug("Ignoring 0 deposit removal")
-		return
-	}
-
-	c.depositsLock.Lock()
-	defer c.depositsLock.Unlock()
-
-	cleanDeposits := make([]*ethpb.DepositContainer, 0, len(c.pendingDeposits))
-	for _, dp := range c.pendingDeposits {
-		if dp.Index >= merkleTreeIndex {
-			cleanDeposits = append(cleanDeposits, dp)
-		}
-	}
-
-	c.pendingDeposits = cleanDeposits
-	pendingDepositsCount.Set(float64(len(c.pendingDeposits)))
-}
-
 // InsertPendingDeposit into the database. If deposit or block number are nil
 // then this method does nothing.
 func (c *Cache) InsertPendingDeposit(ctx context.Context, d *ethpb.Deposit, blockNum uint64, index int64, depositRoot [32]byte) {
--- a/beacon-chain/cache/depositsnapshot/deposit_fetcher_test.go
+++ b/beacon-chain/cache/depositsnapshot/deposit_fetcher_test.go
@@ -44,67 +44,3 @@ func TestPendingDeposits_OK(t *testing.T) {
 	all := dc.PendingDeposits(context.Background(), nil)
 	assert.Equal(t, len(dc.pendingDeposits), len(all), "PendingDeposits(ctx, nil) did not return all deposits")
 }
-
-func TestPrunePendingDeposits_ZeroMerkleIndex(t *testing.T) {
-	dc := Cache{}
-
-	dc.pendingDeposits = []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 2, Index: 2},
-		{Eth1BlockHeight: 4, Index: 4},
-		{Eth1BlockHeight: 6, Index: 6},
-		{Eth1BlockHeight: 8, Index: 8},
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-
-	dc.PrunePendingDeposits(context.Background(), 0)
-	expected := []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 2, Index: 2},
-		{Eth1BlockHeight: 4, Index: 4},
-		{Eth1BlockHeight: 6, Index: 6},
-		{Eth1BlockHeight: 8, Index: 8},
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-	assert.DeepEqual(t, expected, dc.pendingDeposits)
-}
-
-func TestPrunePendingDeposits_OK(t *testing.T) {
-	dc := Cache{}
-
-	dc.pendingDeposits = []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 2, Index: 2},
-		{Eth1BlockHeight: 4, Index: 4},
-		{Eth1BlockHeight: 6, Index: 6},
-		{Eth1BlockHeight: 8, Index: 8},
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-
-	dc.PrunePendingDeposits(context.Background(), 6)
-	expected := []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 6, Index: 6},
-		{Eth1BlockHeight: 8, Index: 8},
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-
-	assert.DeepEqual(t, expected, dc.pendingDeposits)
-
-	dc.pendingDeposits = []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 2, Index: 2},
-		{Eth1BlockHeight: 4, Index: 4},
-		{Eth1BlockHeight: 6, Index: 6},
-		{Eth1BlockHeight: 8, Index: 8},
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-
-	dc.PrunePendingDeposits(context.Background(), 10)
-	expected = []*ethpb.DepositContainer{
-		{Eth1BlockHeight: 10, Index: 10},
-		{Eth1BlockHeight: 12, Index: 12},
-	}
-
-	assert.DeepEqual(t, expected, dc.pendingDeposits)
-}
--- a/beacon-chain/cache/depositsnapshot/deposit_pruner.go
+++ b/beacon-chain/cache/depositsnapshot/deposit_pruner.go
@@ -0,0 +1,88 @@
+package depositsnapshot
+
+import (
+	"context"
+
+	"github.com/prysmaticlabs/prysm/v5/monitoring/tracing/trace"
+	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+)
+
+// PruneProofs removes proofs from all deposits whose index is equal or less than untilDepositIndex.
+func (c *Cache) PruneProofs(ctx context.Context, untilDepositIndex int64) error {
+	_, span := trace.StartSpan(ctx, "Cache.PruneProofs")
+	defer span.End()
+	c.depositsLock.Lock()
+	defer c.depositsLock.Unlock()
+
+	if untilDepositIndex >= int64(len(c.deposits)) {
+		untilDepositIndex = int64(len(c.deposits) - 1)
+	}
+
+	for i := untilDepositIndex; i >= 0; i-- {
+		// Finding a nil proof means that all proofs up to this deposit have been already pruned.
+		if c.deposits[i].Deposit.Proof == nil {
+			break
+		}
+		c.deposits[i].Deposit.Proof = nil
+	}
+
+	return nil
+}
+
+// PruneAllProofs removes proofs from all deposits.
+// As EIP-6110 applies and the legacy deposit mechanism is deprecated,
+// proofs in deposit snapshot are no longer needed.
+// See: https://eips.ethereum.org/EIPS/eip-6110#eth1data-poll-deprecation
+func (c *Cache) PruneAllProofs(ctx context.Context) {
+	_, span := trace.StartSpan(ctx, "Cache.PruneAllProofs")
+	defer span.End()
+
+	c.depositsLock.Lock()
+	defer c.depositsLock.Unlock()
+
+	for i := len(c.deposits) - 1; i >= 0; i-- {
+		if c.deposits[i].Deposit.Proof == nil {
+			break
+		}
+		c.deposits[i].Deposit.Proof = nil
+	}
+}
+
+// PrunePendingDeposits removes any deposit which is older than the given deposit merkle tree index.
+func (c *Cache) PrunePendingDeposits(ctx context.Context, merkleTreeIndex int64) {
+	_, span := trace.StartSpan(ctx, "Cache.PrunePendingDeposits")
+	defer span.End()
+
+	if merkleTreeIndex == 0 {
+		log.Debug("Ignoring 0 deposit removal")
+		return
+	}
+
+	c.depositsLock.Lock()
+	defer c.depositsLock.Unlock()
+
+	cleanDeposits := make([]*ethpb.DepositContainer, 0, len(c.pendingDeposits))
+	for _, dp := range c.pendingDeposits {
+		if dp.Index >= merkleTreeIndex {
+			cleanDeposits = append(cleanDeposits, dp)
+		}
+	}
+
+	c.pendingDeposits = cleanDeposits
+	pendingDepositsCount.Set(float64(len(c.pendingDeposits)))
+}
+
+// PruneAllPendingDeposits removes all pending deposits from the cache.
+// As EIP-6110 applies and the legacy deposit mechanism is deprecated,
+// pending deposits in deposit snapshot are no longer needed.
+// See: https://eips.ethereum.org/EIPS/eip-6110#eth1data-poll-deprecation
+func (c *Cache) PruneAllPendingDeposits(ctx context.Context) {
+	_, span := trace.StartSpan(ctx, "Cache.PruneAllPendingDeposits")
+	defer span.End()
+
+	c.depositsLock.Lock()
+	defer c.depositsLock.Unlock()
+
+	c.pendingDeposits = make([]*ethpb.DepositContainer, 0)
+	pendingDepositsCount.Set(float64(0))
+}
--- a/beacon-chain/cache/depositsnapshot/deposit_pruner_test.go
+++ b/beacon-chain/cache/depositsnapshot/deposit_pruner_test.go
@@ -0,0 +1,323 @@
+package depositsnapshot
+
+import (
+	"context"
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
+	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+	"github.com/prysmaticlabs/prysm/v5/testing/assert"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+)
+
+func TestPrunePendingDeposits_ZeroMerkleIndex(t *testing.T) {
+	dc := Cache{}
+
+	dc.pendingDeposits = []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 2, Index: 2},
+		{Eth1BlockHeight: 4, Index: 4},
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	dc.PrunePendingDeposits(context.Background(), 0)
+	expected := []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 2, Index: 2},
+		{Eth1BlockHeight: 4, Index: 4},
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+	assert.DeepEqual(t, expected, dc.pendingDeposits)
+}
+
+func TestPrunePendingDeposits_OK(t *testing.T) {
+	dc := Cache{}
+
+	dc.pendingDeposits = []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 2, Index: 2},
+		{Eth1BlockHeight: 4, Index: 4},
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	dc.PrunePendingDeposits(context.Background(), 6)
+	expected := []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	assert.DeepEqual(t, expected, dc.pendingDeposits)
+
+	dc.pendingDeposits = []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 2, Index: 2},
+		{Eth1BlockHeight: 4, Index: 4},
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	dc.PrunePendingDeposits(context.Background(), 10)
+	expected = []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	assert.DeepEqual(t, expected, dc.pendingDeposits)
+}
+
+func TestPruneAllPendingDeposits(t *testing.T) {
+	dc := Cache{}
+
+	dc.pendingDeposits = []*ethpb.DepositContainer{
+		{Eth1BlockHeight: 2, Index: 2},
+		{Eth1BlockHeight: 4, Index: 4},
+		{Eth1BlockHeight: 6, Index: 6},
+		{Eth1BlockHeight: 8, Index: 8},
+		{Eth1BlockHeight: 10, Index: 10},
+		{Eth1BlockHeight: 12, Index: 12},
+	}
+
+	dc.PruneAllPendingDeposits(context.Background())
+	expected := []*ethpb.DepositContainer{}
+
+	assert.DeepEqual(t, expected, dc.pendingDeposits)
+}
+
+func TestPruneProofs_Ok(t *testing.T) {
+	dc, err := New()
+	require.NoError(t, err)
+
+	deposits := []struct {
+		blkNum  uint64
+		deposit *ethpb.Deposit
+		index   int64
+	}{
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
+			index: 0,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
+			index: 1,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
+			index: 2,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
+			index: 3,
+		},
+	}
+
+	for _, ins := range deposits {
+		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
+	}
+
+	require.NoError(t, dc.PruneProofs(context.Background(), 1))
+
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
+	assert.NotNil(t, dc.deposits[2].Deposit.Proof)
+	assert.NotNil(t, dc.deposits[3].Deposit.Proof)
+}
+
+func TestPruneProofs_SomeAlreadyPruned(t *testing.T) {
+	dc, err := New()
+	require.NoError(t, err)
+
+	deposits := []struct {
+		blkNum  uint64
+		deposit *ethpb.Deposit
+		index   int64
+	}{
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: nil, Data: &ethpb.Deposit_Data{
+				PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
+			index: 0,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: nil, Data: &ethpb.Deposit_Data{
+				PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}}, index: 1,
+		},
+		{
+			blkNum:  0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(), Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
+			index:   2,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
+			index: 3,
+		},
+	}
+
+	for _, ins := range deposits {
+		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
+	}
+
+	require.NoError(t, dc.PruneProofs(context.Background(), 2))
+
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
+}
+
+func TestPruneProofs_PruneAllWhenDepositIndexTooBig(t *testing.T) {
+	dc, err := New()
+	require.NoError(t, err)
+
+	deposits := []struct {
+		blkNum  uint64
+		deposit *ethpb.Deposit
+		index   int64
+	}{
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
+			index: 0,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
+			index: 1,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
+			index: 2,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
+			index: 3,
+		},
+	}
+
+	for _, ins := range deposits {
+		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
+	}
+
+	require.NoError(t, dc.PruneProofs(context.Background(), 99))
+
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[3].Deposit.Proof)
+}
+
+func TestPruneProofs_CorrectlyHandleLastIndex(t *testing.T) {
+	dc, err := New()
+	require.NoError(t, err)
+
+	deposits := []struct {
+		blkNum  uint64
+		deposit *ethpb.Deposit
+		index   int64
+	}{
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
+			index: 0,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
+			index: 1,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
+			index: 2,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
+			index: 3,
+		},
+	}
+
+	for _, ins := range deposits {
+		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
+	}
+
+	require.NoError(t, dc.PruneProofs(context.Background(), 4))
+
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[3].Deposit.Proof)
+}
+
+func TestPruneAllProofs(t *testing.T) {
+	dc, err := New()
+	require.NoError(t, err)
+
+	deposits := []struct {
+		blkNum  uint64
+		deposit *ethpb.Deposit
+		index   int64
+	}{
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk0"), 48)}},
+			index: 0,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk1"), 48)}},
+			index: 1,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk2"), 48)}},
+			index: 2,
+		},
+		{
+			blkNum: 0,
+			deposit: &ethpb.Deposit{Proof: makeDepositProof(),
+				Data: &ethpb.Deposit_Data{PublicKey: bytesutil.PadTo([]byte("pk3"), 48)}},
+			index: 3,
+		},
+	}
+
+	for _, ins := range deposits {
+		assert.NoError(t, dc.InsertDeposit(context.Background(), ins.deposit, ins.blkNum, ins.index, [32]byte{}))
+	}
+
+	dc.PruneAllProofs(context.Background())
+
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[0].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[1].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[2].Deposit.Proof)
+	assert.DeepEqual(t, [][]byte(nil), dc.deposits[3].Deposit.Proof)
+}
--- a/beacon-chain/cache/interfaces.go
+++ b/beacon-chain/cache/interfaces.go
@@ -12,6 +12,7 @@ import (
 type DepositCache interface {
 	DepositFetcher
 	DepositInserter
+	DepositPruner
 }

 // DepositFetcher defines a struct which can retrieve deposit information from a store.
@@ -23,8 +24,6 @@ type DepositFetcher interface {
 	InsertPendingDeposit(ctx context.Context, d *ethpb.Deposit, blockNum uint64, index int64, depositRoot [32]byte)
 	PendingDeposits(ctx context.Context, untilBlk *big.Int) []*ethpb.Deposit
 	PendingContainers(ctx context.Context, untilBlk *big.Int) []*ethpb.DepositContainer
-	PrunePendingDeposits(ctx context.Context, merkleTreeIndex int64)
-	PruneProofs(ctx context.Context, untilDepositIndex int64) error
 	FinalizedFetcher
 }

@@ -42,6 +41,14 @@ type FinalizedFetcher interface {
 	NonFinalizedDeposits(ctx context.Context, lastFinalizedIndex int64, untilBlk *big.Int) []*ethpb.Deposit
 }

+// DepositPruner is an interface for pruning deposits and proofs.
+type DepositPruner interface {
+	PrunePendingDeposits(ctx context.Context, merkleTreeIndex int64)
+	PruneAllPendingDeposits(ctx context.Context)
+	PruneProofs(ctx context.Context, untilDepositIndex int64) error
+	PruneAllProofs(ctx context.Context)
+}
+
 // FinalizedDeposits defines a method to access a merkle tree containing deposits and their indexes.
 type FinalizedDeposits interface {
 	Deposits() MerkleTree
--- a/beacon-chain/core/blocks/attester_slashing_test.go
+++ b/beacon-chain/core/blocks/attester_slashing_test.go
@@ -7,12 +7,14 @@ import (
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/blocks"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/signing"
 	v "github.com/prysmaticlabs/prysm/v5/beacon-chain/core/validators"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/state"
 	state_native "github.com/prysmaticlabs/prysm/v5/beacon-chain/state/state-native"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/crypto/bls"
 	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+	"github.com/prysmaticlabs/prysm/v5/runtime/version"
 	"github.com/prysmaticlabs/prysm/v5/testing/assert"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 	"github.com/prysmaticlabs/prysm/v5/testing/util"
@@ -105,293 +107,162 @@ func TestProcessAttesterSlashings_IndexedAttestationFailedToVerify(t *testing.T)
 }

 func TestProcessAttesterSlashings_AppliesCorrectStatus(t *testing.T) {
-	beaconState, privKeys := util.DeterministicGenesisState(t, 100)
-	for _, vv := range beaconState.Validators() {
-		vv.WithdrawableEpoch = primitives.Epoch(params.BeaconConfig().SlotsPerEpoch)
-	}
+	statePhase0, keysPhase0 := util.DeterministicGenesisState(t, 100)
+	stateAltair, keysAltair := util.DeterministicGenesisStateAltair(t, 100)
+	stateBellatrix, keysBellatrix := util.DeterministicGenesisStateBellatrix(t, 100)
+	stateCapella, keysCapella := util.DeterministicGenesisStateCapella(t, 100)
+	stateDeneb, keysDeneb := util.DeterministicGenesisStateDeneb(t, 100)
+	stateElectra, keysElectra := util.DeterministicGenesisStateElectra(t, 100)

-	att1 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
+	att1Phase0 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
 		Data: &ethpb.AttestationData{
 			Source: &ethpb.Checkpoint{Epoch: 1},
 		},
 		AttestingIndices: []uint64{0, 1},
 	})
-	domain, err := signing.Domain(beaconState.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, beaconState.GenesisValidatorsRoot())
-	require.NoError(t, err)
-	signingRoot, err := signing.ComputeSigningRoot(att1.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 := privKeys[0].Sign(signingRoot[:])
-	sig1 := privKeys[1].Sign(signingRoot[:])
-	aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att1.Signature = aggregateSig.Marshal()
-
-	att2 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
+	att2Phase0 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
 		AttestingIndices: []uint64{0, 1},
 	})
-	signingRoot, err = signing.ComputeSigningRoot(att2.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 = privKeys[0].Sign(signingRoot[:])
-	sig1 = privKeys[1].Sign(signingRoot[:])
-	aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att2.Signature = aggregateSig.Marshal()
-
-	slashings := []*ethpb.AttesterSlashing{
-		{
-			Attestation_1: att1,
-			Attestation_2: att2,
-		},
-	}
-
-	currentSlot := 2 * params.BeaconConfig().SlotsPerEpoch
-	require.NoError(t, beaconState.SetSlot(currentSlot))
-
-	b := util.NewBeaconBlock()
-	b.Block = &ethpb.BeaconBlock{
-		Body: &ethpb.BeaconBlockBody{
-			AttesterSlashings: slashings,
-		},
-	}
-
-	ss := make([]ethpb.AttSlashing, len(b.Block.Body.AttesterSlashings))
-	for i, s := range b.Block.Body.AttesterSlashings {
-		ss[i] = s
-	}
-	newState, err := blocks.ProcessAttesterSlashings(context.Background(), beaconState, ss, v.SlashValidator)
-	require.NoError(t, err)
-	newRegistry := newState.Validators()
-
-	// Given the intersection of slashable indices is [1], only validator
-	// at index 1 should be slashed and exited. We confirm this below.
-	if newRegistry[1].ExitEpoch != beaconState.Validators()[1].ExitEpoch {
-		t.Errorf(
-			`
-			Expected validator at index 1's exit epoch to match
-			%d, received %d instead
-			`,
-			beaconState.Validators()[1].ExitEpoch,
-			newRegistry[1].ExitEpoch,
-		)
-	}
-
-	require.Equal(t, uint64(31750000000), newState.Balances()[1])
-	require.Equal(t, uint64(32000000000), newState.Balances()[2])
-}
-
-func TestProcessAttesterSlashings_AppliesCorrectStatusAltair(t *testing.T) {
-	beaconState, privKeys := util.DeterministicGenesisStateAltair(t, 100)
-	for _, vv := range beaconState.Validators() {
-		vv.WithdrawableEpoch = primitives.Epoch(params.BeaconConfig().SlotsPerEpoch)
-	}
-
-	att1 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
+	att1Electra := util.HydrateIndexedAttestationElectra(&ethpb.IndexedAttestationElectra{
 		Data: &ethpb.AttestationData{
 			Source: &ethpb.Checkpoint{Epoch: 1},
 		},
 		AttestingIndices: []uint64{0, 1},
 	})
-	domain, err := signing.Domain(beaconState.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, beaconState.GenesisValidatorsRoot())
-	require.NoError(t, err)
-	signingRoot, err := signing.ComputeSigningRoot(att1.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 := privKeys[0].Sign(signingRoot[:])
-	sig1 := privKeys[1].Sign(signingRoot[:])
-	aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att1.Signature = aggregateSig.Marshal()
-
-	att2 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
+	att2Electra := util.HydrateIndexedAttestationElectra(&ethpb.IndexedAttestationElectra{
 		AttestingIndices: []uint64{0, 1},
 	})
-	signingRoot, err = signing.ComputeSigningRoot(att2.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 = privKeys[0].Sign(signingRoot[:])
-	sig1 = privKeys[1].Sign(signingRoot[:])
-	aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att2.Signature = aggregateSig.Marshal()

-	slashings := []*ethpb.AttesterSlashing{
+	slashingPhase0 := &ethpb.AttesterSlashing{
+		Attestation_1: att1Phase0,
+		Attestation_2: att2Phase0,
+	}
+	slashingElectra := &ethpb.AttesterSlashingElectra{
+		Attestation_1: att1Electra,
+		Attestation_2: att2Electra,
+	}
+
+	type testCase struct {
+		name           string
+		st             state.BeaconState
+		keys           []bls.SecretKey
+		att1           ethpb.IndexedAtt
+		att2           ethpb.IndexedAtt
+		slashing       ethpb.AttSlashing
+		slashedBalance uint64
+	}
+
+	testCases := []testCase{
 		{
-			Attestation_1: att1,
-			Attestation_2: att2,
+			name:           "phase0",
+			st:             statePhase0,
+			keys:           keysPhase0,
+			att1:           att1Phase0,
+			att2:           att2Phase0,
+			slashing:       slashingPhase0,
+			slashedBalance: 31750000000,
+		},
+		{
+			name:           "altair",
+			st:             stateAltair,
+			keys:           keysAltair,
+			att1:           att1Phase0,
+			att2:           att2Phase0,
+			slashing:       slashingPhase0,
+			slashedBalance: 31500000000,
+		},
+		{
+			name:           "bellatrix",
+			st:             stateBellatrix,
+			keys:           keysBellatrix,
+			att1:           att1Phase0,
+			att2:           att2Phase0,
+			slashing:       slashingPhase0,
+			slashedBalance: 31000000000,
+		},
+		{
+			name:           "capella",
+			st:             stateCapella,
+			keys:           keysCapella,
+			att1:           att1Phase0,
+			att2:           att2Phase0,
+			slashing:       slashingPhase0,
+			slashedBalance: 31000000000,
+		},
+		{
+			name:           "deneb",
+			st:             stateDeneb,
+			keys:           keysDeneb,
+			att1:           att1Phase0,
+			att2:           att2Phase0,
+			slashing:       slashingPhase0,
+			slashedBalance: 31000000000,
+		},
+		{
+			name:           "electra",
+			st:             stateElectra,
+			keys:           keysElectra,
+			att1:           att1Electra,
+			att2:           att2Electra,
+			slashing:       slashingElectra,
+			slashedBalance: 31992187500,
 		},
 	}

-	currentSlot := 2 * params.BeaconConfig().SlotsPerEpoch
-	require.NoError(t, beaconState.SetSlot(currentSlot))
+	for _, tc := range testCases {
+		t.Run(tc.name, func(t *testing.T) {
+			for _, vv := range tc.st.Validators() {
+				vv.WithdrawableEpoch = primitives.Epoch(params.BeaconConfig().SlotsPerEpoch)
+			}

-	b := util.NewBeaconBlock()
-	b.Block = &ethpb.BeaconBlock{
-		Body: &ethpb.BeaconBlockBody{
-			AttesterSlashings: slashings,
-		},
-	}
+			domain, err := signing.Domain(tc.st.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, tc.st.GenesisValidatorsRoot())
+			require.NoError(t, err)
+			signingRoot, err := signing.ComputeSigningRoot(tc.att1.GetData(), domain)
+			assert.NoError(t, err, "Could not get signing root of beacon block header")
+			sig0 := tc.keys[0].Sign(signingRoot[:])
+			sig1 := tc.keys[1].Sign(signingRoot[:])
+			aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})

-	ss := make([]ethpb.AttSlashing, len(b.Block.Body.AttesterSlashings))
-	for i, s := range b.Block.Body.AttesterSlashings {
-		ss[i] = s
-	}
-	newState, err := blocks.ProcessAttesterSlashings(context.Background(), beaconState, ss, v.SlashValidator)
-	require.NoError(t, err)
-	newRegistry := newState.Validators()
+			if tc.att1.Version() >= version.Electra {
+				tc.att1.(*ethpb.IndexedAttestationElectra).Signature = aggregateSig.Marshal()
+			} else {
+				tc.att1.(*ethpb.IndexedAttestation).Signature = aggregateSig.Marshal()
+			}

-	// Given the intersection of slashable indices is [1], only validator
-	// at index 1 should be slashed and exited. We confirm this below.
-	if newRegistry[1].ExitEpoch != beaconState.Validators()[1].ExitEpoch {
-		t.Errorf(
-			`
+			signingRoot, err = signing.ComputeSigningRoot(tc.att2.GetData(), domain)
+			assert.NoError(t, err, "Could not get signing root of beacon block header")
+			sig0 = tc.keys[0].Sign(signingRoot[:])
+			sig1 = tc.keys[1].Sign(signingRoot[:])
+			aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
+
+			if tc.att2.Version() >= version.Electra {
+				tc.att2.(*ethpb.IndexedAttestationElectra).Signature = aggregateSig.Marshal()
+			} else {
+				tc.att2.(*ethpb.IndexedAttestation).Signature = aggregateSig.Marshal()
+			}
+
+			currentSlot := 2 * params.BeaconConfig().SlotsPerEpoch
+			require.NoError(t, tc.st.SetSlot(currentSlot))
+
+			newState, err := blocks.ProcessAttesterSlashings(context.Background(), tc.st, []ethpb.AttSlashing{tc.slashing}, v.SlashValidator)
+			require.NoError(t, err)
+			newRegistry := newState.Validators()
+
+			// Given the intersection of slashable indices is [1], only validator
+			// at index 1 should be slashed and exited. We confirm this below.
+			if newRegistry[1].ExitEpoch != tc.st.Validators()[1].ExitEpoch {
+				t.Errorf(
+					`
 			Expected validator at index 1's exit epoch to match
 			%d, received %d instead
 			`,
-			beaconState.Validators()[1].ExitEpoch,
-			newRegistry[1].ExitEpoch,
-		)
-	}
+					tc.st.Validators()[1].ExitEpoch,
+					newRegistry[1].ExitEpoch,
+				)
+			}

-	require.Equal(t, uint64(31500000000), newState.Balances()[1])
-	require.Equal(t, uint64(32000000000), newState.Balances()[2])
-}
-
-func TestProcessAttesterSlashings_AppliesCorrectStatusBellatrix(t *testing.T) {
-	beaconState, privKeys := util.DeterministicGenesisStateBellatrix(t, 100)
-	for _, vv := range beaconState.Validators() {
-		vv.WithdrawableEpoch = primitives.Epoch(params.BeaconConfig().SlotsPerEpoch)
-	}
-
-	att1 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
-		Data: &ethpb.AttestationData{
-			Source: &ethpb.Checkpoint{Epoch: 1},
-		},
-		AttestingIndices: []uint64{0, 1},
-	})
-	domain, err := signing.Domain(beaconState.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, beaconState.GenesisValidatorsRoot())
-	require.NoError(t, err)
-	signingRoot, err := signing.ComputeSigningRoot(att1.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 := privKeys[0].Sign(signingRoot[:])
-	sig1 := privKeys[1].Sign(signingRoot[:])
-	aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att1.Signature = aggregateSig.Marshal()
-
-	att2 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
-		AttestingIndices: []uint64{0, 1},
-	})
-	signingRoot, err = signing.ComputeSigningRoot(att2.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 = privKeys[0].Sign(signingRoot[:])
-	sig1 = privKeys[1].Sign(signingRoot[:])
-	aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att2.Signature = aggregateSig.Marshal()
-
-	slashings := []*ethpb.AttesterSlashing{
-		{
-			Attestation_1: att1,
-			Attestation_2: att2,
-		},
-	}
-
-	currentSlot := 2 * params.BeaconConfig().SlotsPerEpoch
-	require.NoError(t, beaconState.SetSlot(currentSlot))
-
-	b := util.NewBeaconBlock()
-	b.Block = &ethpb.BeaconBlock{
-		Body: &ethpb.BeaconBlockBody{
-			AttesterSlashings: slashings,
-		},
-	}
-
-	ss := make([]ethpb.AttSlashing, len(b.Block.Body.AttesterSlashings))
-	for i, s := range b.Block.Body.AttesterSlashings {
-		ss[i] = s
-	}
-	newState, err := blocks.ProcessAttesterSlashings(context.Background(), beaconState, ss, v.SlashValidator)
-	require.NoError(t, err)
-	newRegistry := newState.Validators()
-
-	// Given the intersection of slashable indices is [1], only validator
-	// at index 1 should be slashed and exited. We confirm this below.
-	if newRegistry[1].ExitEpoch != beaconState.Validators()[1].ExitEpoch {
-		t.Errorf(
-			`
-			Expected validator at index 1's exit epoch to match
-			%d, received %d instead
-			`,
-			beaconState.Validators()[1].ExitEpoch,
-			newRegistry[1].ExitEpoch,
-		)
-	}
-
-	require.Equal(t, uint64(31000000000), newState.Balances()[1])
-	require.Equal(t, uint64(32000000000), newState.Balances()[2])
-}
-
-func TestProcessAttesterSlashings_AppliesCorrectStatusCapella(t *testing.T) {
-	beaconState, privKeys := util.DeterministicGenesisStateCapella(t, 100)
-	for _, vv := range beaconState.Validators() {
-		vv.WithdrawableEpoch = primitives.Epoch(params.BeaconConfig().SlotsPerEpoch)
-	}
-
-	att1 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
-		Data: &ethpb.AttestationData{
-			Source: &ethpb.Checkpoint{Epoch: 1},
-		},
-		AttestingIndices: []uint64{0, 1},
-	})
-	domain, err := signing.Domain(beaconState.Fork(), 0, params.BeaconConfig().DomainBeaconAttester, beaconState.GenesisValidatorsRoot())
-	require.NoError(t, err)
-	signingRoot, err := signing.ComputeSigningRoot(att1.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 := privKeys[0].Sign(signingRoot[:])
-	sig1 := privKeys[1].Sign(signingRoot[:])
-	aggregateSig := bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att1.Signature = aggregateSig.Marshal()
-
-	att2 := util.HydrateIndexedAttestation(&ethpb.IndexedAttestation{
-		AttestingIndices: []uint64{0, 1},
-	})
-	signingRoot, err = signing.ComputeSigningRoot(att2.Data, domain)
-	assert.NoError(t, err, "Could not get signing root of beacon block header")
-	sig0 = privKeys[0].Sign(signingRoot[:])
-	sig1 = privKeys[1].Sign(signingRoot[:])
-	aggregateSig = bls.AggregateSignatures([]bls.Signature{sig0, sig1})
-	att2.Signature = aggregateSig.Marshal()
-
-	slashings := []*ethpb.AttesterSlashing{
-		{
-			Attestation_1: att1,
-			Attestation_2: att2,
-		},
-	}
-
-	currentSlot := 2 * params.BeaconConfig().SlotsPerEpoch
-	require.NoError(t, beaconState.SetSlot(currentSlot))
-
-	b := util.NewBeaconBlock()
-	b.Block = &ethpb.BeaconBlock{
-		Body: &ethpb.BeaconBlockBody{
-			AttesterSlashings: slashings,
-		},
-	}
-
-	ss := make([]ethpb.AttSlashing, len(b.Block.Body.AttesterSlashings))
-	for i, s := range b.Block.Body.AttesterSlashings {
-		ss[i] = s
-	}
-	newState, err := blocks.ProcessAttesterSlashings(context.Background(), beaconState, ss, v.SlashValidator)
-	require.NoError(t, err)
-	newRegistry := newState.Validators()
-
-	// Given the intersection of slashable indices is [1], only validator
-	// at index 1 should be slashed and exited. We confirm this below.
-	if newRegistry[1].ExitEpoch != beaconState.Validators()[1].ExitEpoch {
-		t.Errorf(
-			`
-			Expected validator at index 1's exit epoch to match
-			%d, received %d instead
-			`,
-			beaconState.Validators()[1].ExitEpoch,
-			newRegistry[1].ExitEpoch,
-		)
-	}
-
-	require.Equal(t, uint64(31000000000), newState.Balances()[1])
-	require.Equal(t, uint64(32000000000), newState.Balances()[2])
+			require.Equal(t, tc.slashedBalance, newState.Balances()[1])
+			require.Equal(t, uint64(32000000000), newState.Balances()[2])
+		})
+	}
 }
--- a/beacon-chain/core/electra/BUILD.bazel
+++ b/beacon-chain/core/electra/BUILD.bazel
@@ -8,6 +8,7 @@ go_library(
        "consolidations.go",
        "deposits.go",
        "effective_balance_updates.go",
+        "error.go",
        "registry_updates.go",
        "transition.go",
        "transition_no_verify_sig.go",
@@ -55,13 +56,16 @@ go_test(
        "deposit_fuzz_test.go",
        "deposits_test.go",
        "effective_balance_updates_test.go",
+        "error_test.go",
        "export_test.go",
        "registry_updates_test.go",
+        "transition_no_verify_sig_test.go",
        "transition_test.go",
        "upgrade_test.go",
        "validator_test.go",
        "withdrawals_test.go",
    ],
+    data = glob(["testdata/**"]),
    embed = [":go_default_library"],
    deps = [
        "//beacon-chain/core/helpers:go_default_library",
@@ -86,6 +90,7 @@ go_test(
        "@com_github_ethereum_go_ethereum//common:go_default_library",
        "@com_github_ethereum_go_ethereum//common/hexutil:go_default_library",
        "@com_github_google_gofuzz//:go_default_library",
+        "@com_github_pkg_errors//:go_default_library",
        "@com_github_sirupsen_logrus//:go_default_library",
        "@com_github_sirupsen_logrus//hooks/test:go_default_library",
    ],
--- a/beacon-chain/core/electra/churn_test.go
+++ b/beacon-chain/core/electra/churn_test.go
@@ -6,6 +6,7 @@ import (
 	"testing"

 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/electra"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/state"
 	state_native "github.com/prysmaticlabs/prysm/v5/beacon-chain/state/state-native"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
@@ -129,6 +130,57 @@ func TestComputeConsolidationEpochAndUpdateChurn(t *testing.T) {
 			expectedEpoch:                         16,           // Flows into another epoch.
 			expectedConsolidationBalanceToConsume: 200000000000, // 200 ETH
 		},
+		{
+			name: "balance to consume is zero, consolidation balance at limit",
+			state: func(t *testing.T) state.BeaconState {
+				activeBal := 32000000000000000 // 32M ETH
+				s, err := state_native.InitializeFromProtoUnsafeElectra(&eth.BeaconStateElectra{
+					Slot:                          slots.UnsafeEpochStart(10),
+					EarliestConsolidationEpoch:    16,
+					ConsolidationBalanceToConsume: 0,
+					Validators:                    createValidatorsWithTotalActiveBalance(primitives.Gwei(activeBal)),
+				})
+				require.NoError(t, err)
+				return s
+			}(t),
+			consolidationBalance:                  helpers.ConsolidationChurnLimit(32000000000000000),
+			expectedEpoch:                         17, // Flows into another epoch.
+			expectedConsolidationBalanceToConsume: 0,
+		},
+		{
+			name: "consolidation balance equals consolidation balance to consume",
+			state: func(t *testing.T) state.BeaconState {
+				activeBal := 32000000000000000 // 32M ETH
+				s, err := state_native.InitializeFromProtoUnsafeElectra(&eth.BeaconStateElectra{
+					Slot:                          slots.UnsafeEpochStart(10),
+					EarliestConsolidationEpoch:    16,
+					ConsolidationBalanceToConsume: helpers.ConsolidationChurnLimit(32000000000000000),
+					Validators:                    createValidatorsWithTotalActiveBalance(primitives.Gwei(activeBal)),
+				})
+				require.NoError(t, err)
+				return s
+			}(t),
+			consolidationBalance:                  helpers.ConsolidationChurnLimit(32000000000000000),
+			expectedEpoch:                         16,
+			expectedConsolidationBalanceToConsume: 0,
+		},
+		{
+			name: "consolidation balance exceeds limit by one",
+			state: func(t *testing.T) state.BeaconState {
+				activeBal := 32000000000000000 // 32M ETH
+				s, err := state_native.InitializeFromProtoUnsafeElectra(&eth.BeaconStateElectra{
+					Slot:                          slots.UnsafeEpochStart(10),
+					EarliestConsolidationEpoch:    16,
+					ConsolidationBalanceToConsume: 0,
+					Validators:                    createValidatorsWithTotalActiveBalance(primitives.Gwei(activeBal)),
+				})
+				require.NoError(t, err)
+				return s
+			}(t),
+			consolidationBalance:                  helpers.ConsolidationChurnLimit(32000000000000000) + 1,
+			expectedEpoch:                         18, // Flows into another epoch.
+			expectedConsolidationBalanceToConsume: helpers.ConsolidationChurnLimit(32000000000000000) - 1,
+		},
 	}

 	for _, tt := range tests {
--- a/beacon-chain/core/electra/consolidations.go
+++ b/beacon-chain/core/electra/consolidations.go
@@ -185,6 +185,9 @@ func ProcessConsolidationRequests(ctx context.Context, st state.BeaconState, req
 	pcLimit := params.BeaconConfig().PendingConsolidationsLimit

 	for _, cr := range reqs {
+		if cr == nil {
+			return errors.New("nil consolidation request")
+		}
 		if ctx.Err() != nil {
 			return fmt.Errorf("cannot process consolidation requests: %w", ctx.Err())
 		}
@@ -262,7 +265,7 @@ func ProcessConsolidationRequests(ctx context.Context, st state.BeaconState, req
 		if !helpers.IsActiveValidator(srcV, curEpoch) || !helpers.IsActiveValidatorUsingTrie(tgtV, curEpoch) {
 			continue
 		}
-		// Neither validator are exiting.
+		// Neither validator is exiting.
 		if srcV.ExitEpoch != ffe || tgtV.ExitEpoch() != ffe {
 			continue
 		}
--- a/beacon-chain/core/electra/consolidations_test.go
+++ b/beacon-chain/core/electra/consolidations_test.go
@@ -209,7 +209,22 @@ func TestProcessConsolidationRequests(t *testing.T) {
 		state    state.BeaconState
 		reqs     []*enginev1.ConsolidationRequest
 		validate func(*testing.T, state.BeaconState)
+		wantErr  bool
 	}{
+		{
+			name: "nil request",
+			state: func() state.BeaconState {
+				st := &eth.BeaconStateElectra{}
+				s, err := state_native.InitializeFromProtoElectra(st)
+				require.NoError(t, err)
+				return s
+			}(),
+			reqs: []*enginev1.ConsolidationRequest{nil},
+			validate: func(t *testing.T, st state.BeaconState) {
+				require.DeepEqual(t, st, st)
+			},
+			wantErr: true,
+		},
 		{
 			name: "one valid request",
 			state: func() state.BeaconState {
@@ -405,7 +420,13 @@ func TestProcessConsolidationRequests(t *testing.T) {
 	for _, tt := range tests {
 		t.Run(tt.name, func(t *testing.T) {
 			err := electra.ProcessConsolidationRequests(context.TODO(), tt.state, tt.reqs)
-			require.NoError(t, err)
+			if (err != nil) != tt.wantErr {
+				t.Errorf("ProcessWithdrawalRequests() error = %v, wantErr %v", err, tt.wantErr)
+				return
+			}
+			if !tt.wantErr {
+				require.NoError(t, err)
+			}
 			if tt.validate != nil {
 				tt.validate(t, tt.state)
 			}
--- a/beacon-chain/core/electra/deposits.go
+++ b/beacon-chain/core/electra/deposits.go
@@ -385,14 +385,8 @@ func batchProcessNewPendingDeposits(ctx context.Context, state state.BeaconState
 		return errors.Wrap(err, "batch signature verification failed")
 	}

-	pubKeyMap := make(map[[48]byte]struct{}, len(pendingDeposits))
-
 	// Process each deposit individually
 	for _, pendingDeposit := range pendingDeposits {
-		_, found := pubKeyMap[bytesutil.ToBytes48(pendingDeposit.PublicKey)]
-		if !found {
-			pubKeyMap[bytesutil.ToBytes48(pendingDeposit.PublicKey)] = struct{}{}
-		}
 		validSignature := allSignaturesVerified

 		// If batch verification failed, check the individual deposit signature
@@ -410,7 +404,8 @@ func batchProcessNewPendingDeposits(ctx context.Context, state state.BeaconState

 		// Add validator to the registry if the signature is valid
 		if validSignature {
-			if found {
+			_, has := state.ValidatorIndexByPubkey(bytesutil.ToBytes48(pendingDeposit.PublicKey))
+			if has {
 				index, _ := state.ValidatorIndexByPubkey(bytesutil.ToBytes48(pendingDeposit.PublicKey))
 				if err := helpers.IncreaseBalance(state, index, pendingDeposit.Amount); err != nil {
 					return errors.Wrap(err, "could not increase balance")
@@ -592,10 +587,10 @@ func processDepositRequest(beaconState state.BeaconState, request *enginev1.Depo
 	if err != nil {
 		return nil, errors.Wrap(err, "could not get deposit requests start index")
 	}
+	if request == nil {
+		return nil, errors.New("nil deposit request")
+	}
 	if requestsStartIndex == params.BeaconConfig().UnsetDepositRequestsStartIndex {
-		if request == nil {
-			return nil, errors.New("nil deposit request")
-		}
 		if err := beaconState.SetDepositRequestsStartIndex(request.Index); err != nil {
 			return nil, errors.Wrap(err, "could not set deposit requests start index")
 		}
--- a/beacon-chain/core/electra/deposits_test.go
+++ b/beacon-chain/core/electra/deposits_test.go
@@ -333,6 +333,7 @@ func TestProcessDepositRequests(t *testing.T) {
 	st, _ := util.DeterministicGenesisStateElectra(t, 1)
 	sk, err := bls.RandKey()
 	require.NoError(t, err)
+	require.NoError(t, st.SetDepositRequestsStartIndex(1))

 	t.Run("empty requests continues", func(t *testing.T) {
 		newSt, err := electra.ProcessDepositRequests(context.Background(), st, []*enginev1.DepositRequest{})
--- a/beacon-chain/core/electra/error.go
+++ b/beacon-chain/core/electra/error.go
@@ -0,0 +1,16 @@
+package electra
+
+import "github.com/pkg/errors"
+
+type execReqErr struct {
+	error
+}
+
+// IsExecutionRequestError returns true if the error has `execReqErr`.
+func IsExecutionRequestError(e error) bool {
+	if e == nil {
+		return false
+	}
+	var d execReqErr
+	return errors.As(e, &d)
+}
--- a/beacon-chain/core/electra/error_test.go
+++ b/beacon-chain/core/electra/error_test.go
@@ -0,0 +1,45 @@
+package electra
+
+import (
+	"testing"
+
+	"github.com/pkg/errors"
+)
+
+func TestIsExecutionRequestError(t *testing.T) {
+	tests := []struct {
+		name string
+		err  error
+		want bool
+	}{
+		{
+			name: "nil error",
+			err:  nil,
+			want: false,
+		},
+		{
+			name: "random error",
+			err:  errors.New("some error"),
+			want: false,
+		},
+		{
+			name: "execution request error",
+			err:  execReqErr{errors.New("execution request failed")},
+			want: true,
+		},
+		{
+			name: "wrapped execution request error",
+			err:  errors.Wrap(execReqErr{errors.New("execution request failed")}, "wrapped"),
+			want: true,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			got := IsExecutionRequestError(tt.err)
+			if got != tt.want {
+				t.Errorf("IsExecutionRequestError(%v) = %v, want %v", tt.err, got, tt.want)
+			}
+		})
+	}
+}
--- a/beacon-chain/core/electra/transition_no_verify_sig.go
+++ b/beacon-chain/core/electra/transition_no_verify_sig.go
@@ -2,7 +2,6 @@ package electra

 import (
 	"context"
-	"fmt"

 	"github.com/pkg/errors"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/blocks"
@@ -82,16 +81,31 @@ func ProcessOperations(
 	if err != nil {
 		return nil, errors.Wrap(err, "could not get execution requests")
 	}
+	for _, d := range requests.Deposits {
+		if d == nil {
+			return nil, errors.New("nil deposit request")
+		}
+	}
 	st, err = ProcessDepositRequests(ctx, st, requests.Deposits)
 	if err != nil {
-		return nil, errors.Wrap(err, "could not process deposit requests")
+		return nil, execReqErr{errors.Wrap(err, "could not process deposit requests")}
+	}
+	for _, w := range requests.Withdrawals {
+		if w == nil {
+			return nil, errors.New("nil withdrawal request")
+		}
 	}
 	st, err = ProcessWithdrawalRequests(ctx, st, requests.Withdrawals)
 	if err != nil {
-		return nil, errors.Wrap(err, "could not process withdrawal requests")
+		return nil, execReqErr{errors.Wrap(err, "could not process withdrawal requests")}
+	}
+	for _, c := range requests.Consolidations {
+		if c == nil {
+			return nil, errors.New("nil consolidation request")
+		}
 	}
 	if err := ProcessConsolidationRequests(ctx, st, requests.Consolidations); err != nil {
-		return nil, fmt.Errorf("could not process consolidation requests: %w", err)
+		return nil, execReqErr{errors.Wrap(err, "could not process consolidation requests")}
 	}
 	return st, nil
 }
--- a/beacon-chain/core/electra/transition_no_verify_sig_test.go
+++ b/beacon-chain/core/electra/transition_no_verify_sig_test.go
@@ -0,0 +1,61 @@
+package electra_test
+
+import (
+	"context"
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/electra"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
+	enginev1 "github.com/prysmaticlabs/prysm/v5/proto/engine/v1"
+	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+	"github.com/prysmaticlabs/prysm/v5/testing/util"
+)
+
+func TestProcessOperationsWithNilRequests(t *testing.T) {
+	tests := []struct {
+		name      string
+		modifyBlk func(blockElectra *ethpb.SignedBeaconBlockElectra)
+		errMsg    string
+	}{
+		{
+			name: "Nil deposit request",
+			modifyBlk: func(blk *ethpb.SignedBeaconBlockElectra) {
+				blk.Block.Body.ExecutionRequests.Deposits = []*enginev1.DepositRequest{nil}
+			},
+			errMsg: "nil deposit request",
+		},
+		{
+			name: "Nil withdrawal request",
+			modifyBlk: func(blk *ethpb.SignedBeaconBlockElectra) {
+				blk.Block.Body.ExecutionRequests.Withdrawals = []*enginev1.WithdrawalRequest{nil}
+			},
+			errMsg: "nil withdrawal request",
+		},
+		{
+			name: "Nil consolidation request",
+			modifyBlk: func(blk *ethpb.SignedBeaconBlockElectra) {
+				blk.Block.Body.ExecutionRequests.Consolidations = []*enginev1.ConsolidationRequest{nil}
+			},
+			errMsg: "nil consolidation request",
+		},
+	}
+
+	for _, tc := range tests {
+		t.Run(tc.name, func(t *testing.T) {
+			st, ks := util.DeterministicGenesisStateElectra(t, 128)
+			blk, err := util.GenerateFullBlockElectra(st, ks, util.DefaultBlockGenConfig(), 1)
+			require.NoError(t, err)
+
+			tc.modifyBlk(blk)
+
+			b, err := blocks.NewSignedBeaconBlock(blk)
+			require.NoError(t, err)
+
+			require.NoError(t, st.SetSlot(1))
+
+			_, err = electra.ProcessOperations(context.Background(), st, b.Block())
+			require.ErrorContains(t, tc.errMsg, err)
+		})
+	}
+}
--- a/beacon-chain/core/electra/withdrawals_test.go
+++ b/beacon-chain/core/electra/withdrawals_test.go
@@ -38,6 +38,17 @@ func TestProcessWithdrawRequests(t *testing.T) {
 		wantFn  func(t *testing.T, got state.BeaconState)
 		wantErr bool
 	}{
+		{
+			name: "nil request",
+			args: args{
+				st:  func() state.BeaconState { return st }(),
+				wrs: []*enginev1.WithdrawalRequest{nil},
+			},
+			wantErr: true,
+			wantFn: func(t *testing.T, got state.BeaconState) {
+				require.DeepEqual(t, got, nil)
+			},
+		},
 		{
 			name: "happy path exit and withdrawal only",
 			args: args{
--- a/beacon-chain/core/feed/operation/events.go
+++ b/beacon-chain/core/feed/operation/events.go
@@ -32,6 +32,9 @@ const (

 	// AttesterSlashingReceived is sent after an attester slashing is received from gossip or rpc
 	AttesterSlashingReceived = 8
+
+	// SingleAttReceived is sent after a single attestation object is received from gossip or rpc
+	SingleAttReceived = 9
 )

 // UnAggregatedAttReceivedData is the data sent with UnaggregatedAttReceived events.
@@ -43,7 +46,7 @@ type UnAggregatedAttReceivedData struct {
 // AggregatedAttReceivedData is the data sent with AggregatedAttReceived events.
 type AggregatedAttReceivedData struct {
 	// Attestation is the aggregated attestation object.
-	Attestation *ethpb.AggregateAttestationAndProof
+	Attestation ethpb.AggregateAttAndProof
 }

 // ExitReceivedData is the data sent with ExitReceived events.
@@ -77,3 +80,8 @@ type ProposerSlashingReceivedData struct {
 type AttesterSlashingReceivedData struct {
 	AttesterSlashing ethpb.AttSlashing
 }
+
+// SingleAttReceivedData is the data sent with SingleAttReceived events.
+type SingleAttReceivedData struct {
+	Attestation ethpb.Att
+}
--- a/beacon-chain/core/helpers/BUILD.bazel
+++ b/beacon-chain/core/helpers/BUILD.bazel
@@ -7,6 +7,7 @@ go_library(
        "beacon_committee.go",
        "block.go",
        "genesis.go",
+        "legacy.go",
        "metrics.go",
        "randao.go",
        "rewards_penalties.go",
@@ -52,6 +53,7 @@ go_test(
        "attestation_test.go",
        "beacon_committee_test.go",
        "block_test.go",
+        "legacy_test.go",
        "private_access_fuzz_noop_test.go",  # keep
        "private_access_test.go",
        "randao_test.go",
@@ -86,5 +88,6 @@ go_test(
        "//time:go_default_library",
        "//time/slots:go_default_library",
        "@com_github_prysmaticlabs_go_bitfield//:go_default_library",
+        "@com_github_stretchr_testify//require:go_default_library",
    ],
 )
--- a/beacon-chain/core/helpers/legacy.go
+++ b/beacon-chain/core/helpers/legacy.go
@@ -0,0 +1,20 @@
+package helpers
+
+import (
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/state"
+	"github.com/prysmaticlabs/prysm/v5/runtime/version"
+)
+
+// DepositRequestsStarted determines if the deposit requests have started.
+func DepositRequestsStarted(beaconState state.BeaconState) bool {
+	if beaconState.Version() < version.Electra {
+		return false
+	}
+
+	requestsStartIndex, err := beaconState.DepositRequestsStartIndex()
+	if err != nil {
+		return false
+	}
+
+	return beaconState.Eth1DepositIndex() == requestsStartIndex
+}
--- a/beacon-chain/core/helpers/legacy_test.go
+++ b/beacon-chain/core/helpers/legacy_test.go
@@ -0,0 +1,33 @@
+package helpers_test
+
+import (
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
+	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	"github.com/stretchr/testify/require"
+)
+
+// TestDepositRequestHaveStarted contains several test cases for depositRequestHaveStarted.
+func TestDepositRequestHaveStarted(t *testing.T) {
+	t.Run("Version below Electra returns false", func(t *testing.T) {
+		st, _ := util.DeterministicGenesisStateBellatrix(t, 1)
+		result := helpers.DepositRequestsStarted(st)
+		require.False(t, result)
+	})
+
+	t.Run("Version is Electra or higher, no error, but Eth1DepositIndex != requestsStartIndex returns false", func(t *testing.T) {
+		st, _ := util.DeterministicGenesisStateElectra(t, 1)
+		require.NoError(t, st.SetEth1DepositIndex(1))
+		result := helpers.DepositRequestsStarted(st)
+		require.False(t, result)
+	})
+
+	t.Run("Version is Electra or higher, no error, and Eth1DepositIndex == requestsStartIndex returns true", func(t *testing.T) {
+		st, _ := util.DeterministicGenesisStateElectra(t, 1)
+		require.NoError(t, st.SetEth1DepositIndex(33))
+		require.NoError(t, st.SetDepositRequestsStartIndex(33))
+		result := helpers.DepositRequestsStarted(st)
+		require.True(t, result)
+	})
+}
--- a/beacon-chain/core/helpers/validator_churn.go
+++ b/beacon-chain/core/helpers/validator_churn.go
@@ -22,7 +22,7 @@ import (
 func BalanceChurnLimit(activeBalance primitives.Gwei) primitives.Gwei {
 	churn := max(
 		params.BeaconConfig().MinPerEpochChurnLimitElectra,
-		(uint64(activeBalance) / params.BeaconConfig().ChurnLimitQuotient),
+		uint64(activeBalance)/params.BeaconConfig().ChurnLimitQuotient,
 	)
 	return primitives.Gwei(churn - churn%params.BeaconConfig().EffectiveBalanceIncrement)
 }
--- a/beacon-chain/core/helpers/validators.go
+++ b/beacon-chain/core/helpers/validators.go
@@ -393,9 +393,9 @@ func ComputeProposerIndex(bState state.ReadOnlyBeaconState, activeIndices []prim
 		effectiveBal := v.EffectiveBalance()
 		if bState.Version() >= version.Electra {
 			binary.LittleEndian.PutUint64(seedBuffer[len(seed):], i/16)
-			randomByte := hashFunc(seedBuffer)
+			randomBytes := hashFunc(seedBuffer)
 			offset := (i % 16) * 2
-			randomValue := uint64(randomByte[offset]) | uint64(randomByte[offset+1])<<8
+			randomValue := uint64(randomBytes[offset]) | uint64(randomBytes[offset+1])<<8

 			if effectiveBal*fieldparams.MaxRandomValueElectra >= beaconConfig.MaxEffectiveBalanceElectra*randomValue {
 				return candidateIndex, nil
@@ -579,7 +579,7 @@ func IsPartiallyWithdrawableValidator(val state.ReadOnlyValidator, balance uint6
 //	"""
 //	Check if ``validator`` is partially withdrawable.
 //	"""
-//	max_effective_balance = get_validator_max_effective_balance(validator)
+//	max_effective_balance = get_max_effective_balance(validator)
 //	has_max_effective_balance = validator.effective_balance == max_effective_balance  # [Modified in Electra:EIP7251]
 //	has_excess_balance = balance > max_effective_balance  # [Modified in Electra:EIP7251]
 //	return (
@@ -619,7 +619,7 @@ func isPartiallyWithdrawableValidatorCapella(val state.ReadOnlyValidator, balanc
 //
 // Spec definition:
 //
-//	def get_validator_max_effective_balance(validator: Validator) -> Gwei:
+//	def get_max_effective_balance(validator: Validator) -> Gwei:
 //	    """
 //	    Get max effective balance for ``validator``.
 //	    """
--- a/beacon-chain/core/light-client/lightclient_test.go
+++ b/beacon-chain/core/light-client/lightclient_test.go
@@ -22,6 +22,15 @@ import (
 )

 func TestLightClient_NewLightClientOptimisticUpdateFromBeaconState(t *testing.T) {
+	params.SetupTestConfigCleanup(t)
+	cfg := params.BeaconConfig()
+	cfg.AltairForkEpoch = 1
+	cfg.BellatrixForkEpoch = 2
+	cfg.CapellaForkEpoch = 3
+	cfg.DenebForkEpoch = 4
+	cfg.ElectraForkEpoch = 5
+	params.OverrideBeaconConfig(cfg)
+
 	t.Run("Altair", func(t *testing.T) {
 		l := util.NewTestLightClient(t).SetupTestAltair()

@@ -59,9 +68,31 @@ func TestLightClient_NewLightClientOptimisticUpdateFromBeaconState(t *testing.T)
 		l.CheckSyncAggregate(update.SyncAggregate())
 		l.CheckAttestedHeader(update.AttestedHeader())
 	})
+
+	t.Run("Electra", func(t *testing.T) {
+		l := util.NewTestLightClient(t).SetupTestElectra(false)
+
+		update, err := lightClient.NewLightClientOptimisticUpdateFromBeaconState(l.Ctx, l.State.Slot(), l.State, l.Block, l.AttestedState, l.AttestedBlock)
+		require.NoError(t, err)
+		require.NotNil(t, update, "update is nil")
+
+		require.Equal(t, l.Block.Block().Slot(), update.SignatureSlot(), "Signature slot is not equal")
+
+		l.CheckSyncAggregate(update.SyncAggregate())
+		l.CheckAttestedHeader(update.AttestedHeader())
+	})
 }

 func TestLightClient_NewLightClientFinalityUpdateFromBeaconState(t *testing.T) {
+	params.SetupTestConfigCleanup(t)
+	cfg := params.BeaconConfig()
+	cfg.AltairForkEpoch = 1
+	cfg.BellatrixForkEpoch = 2
+	cfg.CapellaForkEpoch = 3
+	cfg.DenebForkEpoch = 4
+	cfg.ElectraForkEpoch = 5
+	params.OverrideBeaconConfig(cfg)
+
 	t.Run("Altair", func(t *testing.T) {
 		l := util.NewTestLightClient(t).SetupTestAltair()

@@ -356,6 +387,157 @@ func TestLightClient_NewLightClientFinalityUpdateFromBeaconState(t *testing.T) {
 			require.DeepSSZEqual(t, execution, updateExecution.Proto(), "Finalized Block Execution is not equal")
 		})
 	})
+
+	t.Run("Electra", func(t *testing.T) {
+		t.Run("FinalizedBlock Not Nil", func(t *testing.T) {
+			l := util.NewTestLightClient(t).SetupTestElectra(false)
+
+			update, err := lightClient.NewLightClientFinalityUpdateFromBeaconState(l.Ctx, l.State.Slot(), l.State, l.Block, l.AttestedState, l.AttestedBlock, l.FinalizedBlock)
+			require.NoError(t, err)
+			require.NotNil(t, update, "update is nil")
+
+			require.Equal(t, l.Block.Block().Slot(), update.SignatureSlot(), "Signature slot is not equal")
+
+			l.CheckSyncAggregate(update.SyncAggregate())
+			l.CheckAttestedHeader(update.AttestedHeader())
+
+			//zeroHash := params.BeaconConfig().ZeroHash[:]
+			finalizedBlockHeader, err := l.FinalizedBlock.Header()
+			require.NoError(t, err)
+			require.NotNil(t, update.FinalizedHeader(), "Finalized header is nil")
+			updateFinalizedHeaderBeacon := update.FinalizedHeader().Beacon()
+			require.Equal(t, finalizedBlockHeader.Header.Slot, updateFinalizedHeaderBeacon.Slot, "Finalized header slot is not equal")
+			require.Equal(t, finalizedBlockHeader.Header.ProposerIndex, updateFinalizedHeaderBeacon.ProposerIndex, "Finalized header proposer index is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.ParentRoot, updateFinalizedHeaderBeacon.ParentRoot, "Finalized header parent root is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.StateRoot, updateFinalizedHeaderBeacon.StateRoot, "Finalized header state root is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.BodyRoot, updateFinalizedHeaderBeacon.BodyRoot, "Finalized header body root is not equal")
+			fb, err := update.FinalityBranchElectra()
+			require.NoError(t, err)
+			proof, err := l.AttestedState.FinalizedRootProof(l.Ctx)
+			require.NoError(t, err)
+			for i, leaf := range fb {
+				require.DeepSSZEqual(t, proof[i], leaf[:], "Leaf is not equal")
+			}
+
+			// Check Execution BlockHash
+			payloadInterface, err := l.FinalizedBlock.Block().Body().Execution()
+			require.NoError(t, err)
+			transactionsRoot, err := payloadInterface.TransactionsRoot()
+			if errors.Is(err, consensustypes.ErrUnsupportedField) {
+				transactions, err := payloadInterface.Transactions()
+				require.NoError(t, err)
+				transactionsRootArray, err := ssz.TransactionsRoot(transactions)
+				require.NoError(t, err)
+				transactionsRoot = transactionsRootArray[:]
+			} else {
+				require.NoError(t, err)
+			}
+			withdrawalsRoot, err := payloadInterface.WithdrawalsRoot()
+			if errors.Is(err, consensustypes.ErrUnsupportedField) {
+				withdrawals, err := payloadInterface.Withdrawals()
+				require.NoError(t, err)
+				withdrawalsRootArray, err := ssz.WithdrawalSliceRoot(withdrawals, fieldparams.MaxWithdrawalsPerPayload)
+				require.NoError(t, err)
+				withdrawalsRoot = withdrawalsRootArray[:]
+			} else {
+				require.NoError(t, err)
+			}
+			execution := &v11.ExecutionPayloadHeaderDeneb{
+				ParentHash:       payloadInterface.ParentHash(),
+				FeeRecipient:     payloadInterface.FeeRecipient(),
+				StateRoot:        payloadInterface.StateRoot(),
+				ReceiptsRoot:     payloadInterface.ReceiptsRoot(),
+				LogsBloom:        payloadInterface.LogsBloom(),
+				PrevRandao:       payloadInterface.PrevRandao(),
+				BlockNumber:      payloadInterface.BlockNumber(),
+				GasLimit:         payloadInterface.GasLimit(),
+				GasUsed:          payloadInterface.GasUsed(),
+				Timestamp:        payloadInterface.Timestamp(),
+				ExtraData:        payloadInterface.ExtraData(),
+				BaseFeePerGas:    payloadInterface.BaseFeePerGas(),
+				BlockHash:        payloadInterface.BlockHash(),
+				TransactionsRoot: transactionsRoot,
+				WithdrawalsRoot:  withdrawalsRoot,
+			}
+			updateExecution, err := update.FinalizedHeader().Execution()
+			require.NoError(t, err)
+			require.DeepSSZEqual(t, execution, updateExecution.Proto(), "Finalized Block Execution is not equal")
+		})
+
+		t.Run("FinalizedBlock In Previous Fork", func(t *testing.T) {
+			l := util.NewTestLightClient(t).SetupTestElectraFinalizedBlockDeneb(false)
+
+			update, err := lightClient.NewLightClientFinalityUpdateFromBeaconState(l.Ctx, l.State.Slot(), l.State, l.Block, l.AttestedState, l.AttestedBlock, l.FinalizedBlock)
+			require.NoError(t, err)
+			require.NotNil(t, update, "update is nil")
+
+			require.Equal(t, l.Block.Block().Slot(), update.SignatureSlot(), "Signature slot is not equal")
+
+			l.CheckSyncAggregate(update.SyncAggregate())
+			l.CheckAttestedHeader(update.AttestedHeader())
+
+			finalizedBlockHeader, err := l.FinalizedBlock.Header()
+			require.NoError(t, err)
+			require.NotNil(t, update.FinalizedHeader(), "Finalized header is nil")
+			updateFinalizedHeaderBeacon := update.FinalizedHeader().Beacon()
+			require.Equal(t, finalizedBlockHeader.Header.Slot, updateFinalizedHeaderBeacon.Slot, "Finalized header slot is not equal")
+			require.Equal(t, finalizedBlockHeader.Header.ProposerIndex, updateFinalizedHeaderBeacon.ProposerIndex, "Finalized header proposer index is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.ParentRoot, updateFinalizedHeaderBeacon.ParentRoot, "Finalized header parent root is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.StateRoot, updateFinalizedHeaderBeacon.StateRoot, "Finalized header state root is not equal")
+			require.DeepSSZEqual(t, finalizedBlockHeader.Header.BodyRoot, updateFinalizedHeaderBeacon.BodyRoot, "Finalized header body root is not equal")
+			fb, err := update.FinalityBranchElectra()
+			require.NoError(t, err)
+			proof, err := l.AttestedState.FinalizedRootProof(l.Ctx)
+			require.NoError(t, err)
+			for i, leaf := range fb {
+				require.DeepSSZEqual(t, proof[i], leaf[:], "Leaf is not equal")
+			}
+
+			// Check Execution BlockHash
+			payloadInterface, err := l.FinalizedBlock.Block().Body().Execution()
+			require.NoError(t, err)
+			transactionsRoot, err := payloadInterface.TransactionsRoot()
+			if errors.Is(err, consensustypes.ErrUnsupportedField) {
+				transactions, err := payloadInterface.Transactions()
+				require.NoError(t, err)
+				transactionsRootArray, err := ssz.TransactionsRoot(transactions)
+				require.NoError(t, err)
+				transactionsRoot = transactionsRootArray[:]
+			} else {
+				require.NoError(t, err)
+			}
+			withdrawalsRoot, err := payloadInterface.WithdrawalsRoot()
+			if errors.Is(err, consensustypes.ErrUnsupportedField) {
+				withdrawals, err := payloadInterface.Withdrawals()
+				require.NoError(t, err)
+				withdrawalsRootArray, err := ssz.WithdrawalSliceRoot(withdrawals, fieldparams.MaxWithdrawalsPerPayload)
+				require.NoError(t, err)
+				withdrawalsRoot = withdrawalsRootArray[:]
+			} else {
+				require.NoError(t, err)
+			}
+			execution := &v11.ExecutionPayloadHeaderDeneb{
+				ParentHash:       payloadInterface.ParentHash(),
+				FeeRecipient:     payloadInterface.FeeRecipient(),
+				StateRoot:        payloadInterface.StateRoot(),
+				ReceiptsRoot:     payloadInterface.ReceiptsRoot(),
+				LogsBloom:        payloadInterface.LogsBloom(),
+				PrevRandao:       payloadInterface.PrevRandao(),
+				BlockNumber:      payloadInterface.BlockNumber(),
+				GasLimit:         payloadInterface.GasLimit(),
+				GasUsed:          payloadInterface.GasUsed(),
+				Timestamp:        payloadInterface.Timestamp(),
+				ExtraData:        payloadInterface.ExtraData(),
+				BaseFeePerGas:    payloadInterface.BaseFeePerGas(),
+				BlockHash:        payloadInterface.BlockHash(),
+				TransactionsRoot: transactionsRoot,
+				WithdrawalsRoot:  withdrawalsRoot,
+			}
+			updateExecution, err := update.FinalizedHeader().Execution()
+			require.NoError(t, err)
+			require.DeepSSZEqual(t, execution, updateExecution.Proto(), "Finalized Block Execution is not equal")
+		})
+	})
 }

 func TestLightClient_BlockToLightClientHeader(t *testing.T) {
--- a/beacon-chain/core/transition/transition.go
+++ b/beacon-chain/core/transition/transition.go
@@ -403,11 +403,15 @@ func VerifyOperationLengths(_ context.Context, state state.BeaconState, b interf
 		)
 	}

-	if uint64(len(body.AttesterSlashings())) > params.BeaconConfig().MaxAttesterSlashings {
+	maxSlashings := params.BeaconConfig().MaxAttesterSlashings
+	if body.Version() >= version.Electra {
+		maxSlashings = params.BeaconConfig().MaxAttesterSlashingsElectra
+	}
+	if uint64(len(body.AttesterSlashings())) > maxSlashings {
 		return nil, fmt.Errorf(
 			"number of attester slashings (%d) in block body exceeds allowed threshold of %d",
 			len(body.AttesterSlashings()),
-			params.BeaconConfig().MaxAttesterSlashings,
+			maxSlashings,
 		)
 	}

--- a/beacon-chain/core/transition/transition_test.go
+++ b/beacon-chain/core/transition/transition_test.go
@@ -437,6 +437,25 @@ func TestProcessBlock_OverMaxAttesterSlashings(t *testing.T) {
 	assert.ErrorContains(t, want, err)
 }

+func TestProcessBlock_OverMaxAttesterSlashingsElectra(t *testing.T) {
+	maxSlashings := params.BeaconConfig().MaxAttesterSlashingsElectra
+	b := &ethpb.SignedBeaconBlockElectra{
+		Block: &ethpb.BeaconBlockElectra{
+			Body: &ethpb.BeaconBlockBodyElectra{
+				AttesterSlashings: make([]*ethpb.AttesterSlashingElectra, maxSlashings+1),
+			},
+		},
+	}
+	want := fmt.Sprintf("number of attester slashings (%d) in block body exceeds allowed threshold of %d",
+		len(b.Block.Body.AttesterSlashings), params.BeaconConfig().MaxAttesterSlashingsElectra)
+	s, err := state_native.InitializeFromProtoUnsafeElectra(&ethpb.BeaconStateElectra{})
+	require.NoError(t, err)
+	wsb, err := consensusblocks.NewSignedBeaconBlock(b)
+	require.NoError(t, err)
+	_, err = transition.VerifyOperationLengths(context.Background(), s, wsb.Block())
+	assert.ErrorContains(t, want, err)
+}
+
 func TestProcessBlock_OverMaxAttestations(t *testing.T) {
 	b := &ethpb.SignedBeaconBlock{
 		Block: &ethpb.BeaconBlock{
--- a/beacon-chain/core/validators/validator.go
+++ b/beacon-chain/core/validators/validator.go
@@ -75,7 +75,7 @@ func InitiateValidatorExit(ctx context.Context, s state.BeaconState, idx primiti

 	// Compute exit queue epoch.
 	if s.Version() < version.Electra {
-		// Relevant spec code from deneb:
+		// Relevant spec code from phase0:
 		//
 		//	exit_epochs = [v.exit_epoch for v in state.validators if v.exit_epoch != FAR_FUTURE_EPOCH]
 		//	exit_queue_epoch = max(exit_epochs + [compute_activation_exit_epoch(get_current_epoch(state))])
--- a/beacon-chain/das/availability.go
+++ b/beacon-chain/das/availability.go
@@ -94,14 +94,7 @@ func (s *LazilyPersistentStore) IsDataAvailable(ctx context.Context, current pri
 	entry := s.cache.ensure(key)
 	defer s.cache.delete(key)
 	root := b.Root()
-	sumz, err := s.store.WaitForSummarizer(ctx)
-	if err != nil {
-		log.WithField("root", fmt.Sprintf("%#x", b.Root())).
-			WithError(err).
-			Debug("Failed to receive BlobStorageSummarizer within IsDataAvailable")
-	} else {
-		entry.setDiskSummary(sumz.Summary(root))
-	}
+	entry.setDiskSummary(s.store.Summary(root))

 	// Verify we have all the expected sidecars, and fail fast if any are missing or inconsistent.
 	// We don't try to salvage problematic batches because this indicates a misbehaving peer and we'd rather
--- a/beacon-chain/db/filesystem/BUILD.bazel
+++ b/beacon-chain/db/filesystem/BUILD.bazel
@@ -5,6 +5,10 @@ go_library(
    srcs = [
        "blob.go",
        "cache.go",
+        "iteration.go",
+        "layout.go",
+        "layout_by_epoch.go",
+        "layout_flat.go",
        "log.go",
        "metrics.go",
        "mock.go",
@@ -13,6 +17,7 @@ go_library(
    importpath = "github.com/prysmaticlabs/prysm/v5/beacon-chain/db/filesystem",
    visibility = ["//visibility:public"],
    deps = [
+        "//beacon-chain/db:go_default_library",
        "//beacon-chain/verification:go_default_library",
        "//config/fieldparams:go_default_library",
        "//config/params:go_default_library",
@@ -20,7 +25,6 @@ go_library(
        "//consensus-types/primitives:go_default_library",
        "//encoding/bytesutil:go_default_library",
        "//io/file:go_default_library",
-        "//proto/prysm/v1alpha1:go_default_library",
        "//runtime/logging:go_default_library",
        "//time/slots:go_default_library",
        "@com_github_ethereum_go_ethereum//common/hexutil:go_default_library",
@@ -37,10 +41,14 @@ go_test(
    srcs = [
        "blob_test.go",
        "cache_test.go",
+        "iteration_test.go",
+        "layout_test.go",
+        "migration_test.go",
        "pruner_test.go",
    ],
    embed = [":go_default_library"],
    deps = [
+        "//beacon-chain/db:go_default_library",
        "//beacon-chain/verification:go_default_library",
        "//config/params:go_default_library",
        "//consensus-types/primitives:go_default_library",
@@ -48,6 +56,7 @@ go_test(
        "//proto/prysm/v1alpha1:go_default_library",
        "//testing/require:go_default_library",
        "//testing/util:go_default_library",
+        "//time/slots:go_default_library",
        "@com_github_prysmaticlabs_fastssz//:go_default_library",
        "@com_github_spf13_afero//:go_default_library",
    ],
--- a/beacon-chain/db/filesystem/blob.go
+++ b/beacon-chain/db/filesystem/blob.go
@@ -1,42 +1,31 @@
 package filesystem

 import (
-	"context"
 	"fmt"
 	"math"
 	"os"
 	"path"
-	"strconv"
-	"strings"
 	"time"

-	"github.com/ethereum/go-ethereum/common/hexutil"
 	"github.com/pkg/errors"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/verification"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
-	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	"github.com/prysmaticlabs/prysm/v5/io/file"
-	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
 	"github.com/prysmaticlabs/prysm/v5/runtime/logging"
 	"github.com/sirupsen/logrus"
 	"github.com/spf13/afero"
 )

+func directoryPermissions() os.FileMode {
+	return params.BeaconIoConfig().ReadWriteExecutePermissions
+}
+
 var (
-	errIndexOutOfBounds    = errors.New("blob index in file name >= DeprecatedMaxBlobsPerBlock")
-	errEmptyBlobWritten    = errors.New("zero bytes written to disk when saving blob sidecar")
+	errIndexOutOfBounds    = errors.New("blob index in file name >= MAX_BLOBS_PER_BLOCK")
 	errSidecarEmptySSZData = errors.New("sidecar marshalled to an empty ssz byte slice")
 	errNoBasePath          = errors.New("BlobStorage base path not specified in init")
-	errInvalidRootString   = errors.New("Could not parse hex string as a [32]byte")
-)
-
-const (
-	sszExt  = "ssz"
-	partExt = "part"
-
-	directoryPermissions = 0700
 )

 // BlobStorageOption is a functional option for configuring a BlobStorage.
@@ -66,6 +55,23 @@ func WithSaveFsync(fsync bool) BlobStorageOption {
 	}
 }

+// WithFs allows the afero.Fs implementation to be customized. Used by tests
+// to substitute an in-memory filesystem.
+func WithFs(fs afero.Fs) BlobStorageOption {
+	return func(b *BlobStorage) error {
+		b.fs = fs
+		return nil
+	}
+}
+
+// WithLayout enables the user to specify which layout scheme to use, dictating how blob files are stored on disk.
+func WithLayout(name string) BlobStorageOption {
+	return func(b *BlobStorage) error {
+		b.layoutName = name
+		return nil
+	}
+}
+
 // NewBlobStorage creates a new instance of the BlobStorage object. Note that the implementation of BlobStorage may
 // attempt to hold a file lock to guarantee exclusive control of the blob storage directory, so this should only be
 // initialized once per beacon node.
@@ -76,19 +82,27 @@ func NewBlobStorage(opts ...BlobStorageOption) (*BlobStorage, error) {
 			return nil, errors.Wrap(err, "failed to create blob storage")
 		}
 	}
-	if b.base == "" {
-		return nil, errNoBasePath
+	// Allow tests to set up a different fs using WithFs.
+	if b.fs == nil {
+		if b.base == "" {
+			return nil, errNoBasePath
+		}
+		b.base = path.Clean(b.base)
+		if err := file.MkdirAll(b.base); err != nil {
+			return nil, errors.Wrapf(err, "failed to create blob storage at %s", b.base)
+		}
+		b.fs = afero.NewBasePathFs(afero.NewOsFs(), b.base)
 	}
-	b.base = path.Clean(b.base)
-	if err := file.MkdirAll(b.base); err != nil {
-		return nil, errors.Wrapf(err, "failed to create blob storage at %s", b.base)
+	b.cache = newBlobStorageCache()
+	pruner := newBlobPruner(b.retentionEpochs)
+	if b.layoutName == "" {
+		b.layoutName = LayoutNameFlat
 	}
-	b.fs = afero.NewBasePathFs(afero.NewOsFs(), b.base)
-	pruner, err := newBlobPruner(b.fs, b.retentionEpochs)
+	layout, err := newLayout(b.layoutName, b.fs, b.cache, pruner)
 	if err != nil {
 		return nil, err
 	}
-	b.pruner = pruner
+	b.layout = layout
 	return b, nil
 }

@@ -96,47 +110,103 @@ func NewBlobStorage(opts ...BlobStorageOption) (*BlobStorage, error) {
 type BlobStorage struct {
 	base            string
 	retentionEpochs primitives.Epoch
+	layoutName      string
 	fsync           bool
 	fs              afero.Fs
-	pruner          *blobPruner
+	layout          fsLayout
+	cache           *blobStorageSummaryCache
 }

 // WarmCache runs the prune routine with an expiration of slot of 0, so nothing will be pruned, but the pruner's cache
 // will be populated at node startup, avoiding a costly cold prune (~4s in syscalls) during syncing.
 func (bs *BlobStorage) WarmCache() {
-	if bs.pruner == nil {
-		return
-	}
-	go func() {
-		start := time.Now()
+	start := time.Now()
+	if bs.layoutName == LayoutNameFlat {
 		log.Info("Blob filesystem cache warm-up started. This may take a few minutes.")
-		if err := bs.pruner.warmCache(); err != nil {
-			log.WithError(err).Error("Error encountered while warming up blob pruner cache")
-		}
-		log.WithField("elapsed", time.Since(start)).Info("Blob filesystem cache warm-up complete")
-	}()
+	} else {
+		log.Info("Blob filesystem cache warm-up started.")
+	}
+
+	if err := warmCache(bs.layout, bs.cache); err != nil {
+		log.WithError(err).Error("Error encountered while warming up blob filesystem cache.")
+	}
+	if err := bs.migrateLayouts(); err != nil {
+		log.WithError(err).Error("Error encountered while migrating blob storage.")
+	}
+	log.WithField("elapsed", time.Since(start)).Info("Blob filesystem cache warm-up complete.")
 }

-// ErrBlobStorageSummarizerUnavailable is a sentinel error returned when there is no pruner/cache available.
-// This should be used by code that optionally uses the summarizer to optimize rpc requests. Being able to
-// fallback when there is no summarizer allows client code to avoid test complexity where the summarizer doesn't matter.
-var ErrBlobStorageSummarizerUnavailable = errors.New("BlobStorage not initialized with a pruner or cache")
-
-// WaitForSummarizer blocks until the BlobStorageSummarizer is ready to use.
-// BlobStorageSummarizer is not ready immediately on node startup because it needs to sample the blob filesystem to
-// determine which blobs are available.
-func (bs *BlobStorage) WaitForSummarizer(ctx context.Context) (BlobStorageSummarizer, error) {
-	if bs == nil || bs.pruner == nil {
-		return nil, ErrBlobStorageSummarizerUnavailable
+// If any blob storage directories are found for layouts besides the configured layout, migrate them.
+func (bs *BlobStorage) migrateLayouts() error {
+	for _, name := range LayoutNames {
+		if name == bs.layoutName {
+			continue
+		}
+		from, err := newLayout(name, bs.fs, bs.cache, nil)
+		if err != nil {
+			return err
+		}
+		if err := migrateLayout(bs.fs, from, bs.layout, bs.cache); err != nil {
+			if errors.Is(err, errLayoutNotDetected) {
+				continue
+			}
+			return errors.Wrapf(err, "failed to migrate layout from %s to %s", name, bs.layoutName)
+		}
 	}
-	return bs.pruner.waitForCache(ctx)
+	return nil
+}
+
+func (bs *BlobStorage) writePart(sidecar blocks.VerifiedROBlob) (ppath string, err error) {
+	ident := identForSidecar(sidecar)
+	sidecarData, err := sidecar.MarshalSSZ()
+	if err != nil {
+		return "", errors.Wrap(err, "failed to serialize sidecar data")
+	}
+	if len(sidecarData) == 0 {
+		return "", errSidecarEmptySSZData
+	}
+
+	if err := bs.fs.MkdirAll(bs.layout.dir(ident), directoryPermissions()); err != nil {
+		return "", err
+	}
+	ppath = bs.layout.partPath(ident, fmt.Sprintf("%p", sidecarData))
+
+	// Create a partial file and write the serialized data to it.
+	partialFile, err := bs.fs.Create(ppath)
+	if err != nil {
+		return "", errors.Wrap(err, "failed to create partial file")
+	}
+	defer func() {
+		cerr := partialFile.Close()
+		// The close error is probably less important than any existing error, so only overwrite nil err.
+		if cerr != nil && err == nil {
+			err = cerr
+		}
+	}()
+
+	n, err := partialFile.Write(sidecarData)
+	if err != nil {
+		return ppath, errors.Wrap(err, "failed to write to partial file")
+	}
+	if bs.fsync {
+		if err := partialFile.Sync(); err != nil {
+			return ppath, err
+		}
+	}
+
+	if n != len(sidecarData) {
+		return ppath, fmt.Errorf("failed to write the full bytes of sidecarData, wrote only %d of %d bytes", n, len(sidecarData))
+	}
+
+	return ppath, nil
 }

 // Save saves blobs given a list of sidecars.
 func (bs *BlobStorage) Save(sidecar blocks.VerifiedROBlob) error {
 	startTime := time.Now()
-	fname := namerForSidecar(sidecar)
-	sszPath := fname.path()
+
+	ident := identForSidecar(sidecar)
+	sszPath := bs.layout.sszPath(ident)
 	exists, err := afero.Exists(bs.fs, sszPath)
 	if err != nil {
 		return err
@@ -145,78 +215,36 @@ func (bs *BlobStorage) Save(sidecar blocks.VerifiedROBlob) error {
 		log.WithFields(logging.BlobFields(sidecar.ROBlob)).Debug("Ignoring a duplicate blob sidecar save attempt")
 		return nil
 	}
-	if bs.pruner != nil {
-		if err := bs.pruner.notify(sidecar.BlockRoot(), sidecar.Slot(), sidecar.Index); err != nil {
-			return errors.Wrapf(err, "problem maintaining pruning cache/metrics for sidecar with root=%#x", sidecar.BlockRoot())
-		}
-	}
-
-	// Serialize the ethpb.BlobSidecar to binary data using SSZ.
-	sidecarData, err := sidecar.MarshalSSZ()
-	if err != nil {
-		return errors.Wrap(err, "failed to serialize sidecar data")
-	} else if len(sidecarData) == 0 {
-		return errSidecarEmptySSZData
-	}
-
-	if err := bs.fs.MkdirAll(fname.dir(), directoryPermissions); err != nil {
-		return err
-	}
-	partPath := fname.partPath(fmt.Sprintf("%p", sidecarData))

 	partialMoved := false
+	partPath, err := bs.writePart(sidecar)
 	// Ensure the partial file is deleted.
 	defer func() {
-		if partialMoved {
+		if partialMoved || partPath == "" {
 			return
 		}
 		// It's expected to error if the save is successful.
-		err = bs.fs.Remove(partPath)
+		err := bs.fs.Remove(partPath)
 		if err == nil {
 			log.WithFields(logrus.Fields{
 				"partPath": partPath,
 			}).Debugf("Removed partial file")
 		}
 	}()
-
-	// Create a partial file and write the serialized data to it.
-	partialFile, err := bs.fs.Create(partPath)
 	if err != nil {
-		return errors.Wrap(err, "failed to create partial file")
-	}
-
-	n, err := partialFile.Write(sidecarData)
-	if err != nil {
-		closeErr := partialFile.Close()
-		if closeErr != nil {
-			return closeErr
-		}
-		return errors.Wrap(err, "failed to write to partial file")
-	}
-	if bs.fsync {
-		if err := partialFile.Sync(); err != nil {
-			return err
-		}
-	}
-
-	if err := partialFile.Close(); err != nil {
 		return err
 	}

-	if n != len(sidecarData) {
-		return fmt.Errorf("failed to write the full bytes of sidecarData, wrote only %d of %d bytes", n, len(sidecarData))
-	}
-
-	if n == 0 {
-		return errEmptyBlobWritten
-	}
-
 	// Atomically rename the partial file to its final name.
 	err = bs.fs.Rename(partPath, sszPath)
 	if err != nil {
 		return errors.Wrap(err, "failed to rename partial file to final name")
 	}
 	partialMoved = true
+
+	if err := bs.layout.notify(ident); err != nil {
+		return errors.Wrapf(err, "problem maintaining pruning cache/metrics for sidecar with root=%#x", sidecar.BlockRoot())
+	}
 	blobsWrittenCounter.Inc()
 	blobSaveLatency.Observe(float64(time.Since(startTime).Milliseconds()))

@@ -228,70 +256,30 @@ func (bs *BlobStorage) Save(sidecar blocks.VerifiedROBlob) error {
 // value is always a VerifiedROBlob.
 func (bs *BlobStorage) Get(root [32]byte, idx uint64) (blocks.VerifiedROBlob, error) {
 	startTime := time.Now()
-	expected := blobNamer{root: root, index: idx}
-	encoded, err := afero.ReadFile(bs.fs, expected.path())
-	var v blocks.VerifiedROBlob
+	ident, err := bs.layout.ident(root, idx)
 	if err != nil {
-		return v, err
-	}
-	s := &ethpb.BlobSidecar{}
-	if err := s.UnmarshalSSZ(encoded); err != nil {
-		return v, err
-	}
-	ro, err := blocks.NewROBlobWithRoot(s, root)
-	if err != nil {
-		return blocks.VerifiedROBlob{}, err
+		return verification.VerifiedROBlobError(err)
 	}
 	defer func() {
 		blobFetchLatency.Observe(float64(time.Since(startTime).Milliseconds()))
 	}()
-	return verification.BlobSidecarNoop(ro)
+	return verification.VerifiedROBlobFromDisk(bs.fs, root, bs.layout.sszPath(ident))
 }

 // Remove removes all blobs for a given root.
 func (bs *BlobStorage) Remove(root [32]byte) error {
-	rootDir := blobNamer{root: root}.dir()
-	return bs.fs.RemoveAll(rootDir)
+	dirIdent, err := bs.layout.dirIdent(root)
+	if err != nil {
+		return err
+	}
+	_, err = bs.layout.remove(dirIdent)
+	return err
 }

-// Indices generates a bitmap representing which BlobSidecar.Index values are present on disk for a given root.
-// This value can be compared to the commitments observed in a block to determine which indices need to be found
-// on the network to confirm data availability.
-func (bs *BlobStorage) Indices(root [32]byte, s primitives.Slot) ([]bool, error) {
-	maxBlobsPerBlock := params.BeaconConfig().MaxBlobsPerBlock(s)
-	mask := make([]bool, maxBlobsPerBlock)
-
-	rootDir := blobNamer{root: root}.dir()
-	entries, err := afero.ReadDir(bs.fs, rootDir)
-	if err != nil {
-		if os.IsNotExist(err) {
-			return mask, nil
-		}
-		return mask, err
-	}
-
-	for i := range entries {
-		if entries[i].IsDir() {
-			continue
-		}
-		name := entries[i].Name()
-		if !strings.HasSuffix(name, sszExt) {
-			continue
-		}
-		parts := strings.Split(name, ".")
-		if len(parts) != 2 {
-			continue
-		}
-		u, err := strconv.ParseUint(parts[0], 10, 64)
-		if err != nil {
-			return mask, errors.Wrapf(err, "unexpected directory entry breaks listing, %s", parts[0])
-		}
-		if u >= uint64(maxBlobsPerBlock) {
-			return mask, errIndexOutOfBounds
-		}
-		mask[u] = true
-	}
-	return mask, nil
+// Summary returns the BlobStorageSummary from the layout.
+// Internally, this is a cached representation of the directory listing for the given root.
+func (bs *BlobStorage) Summary(root [32]byte) BlobStorageSummary {
+	return bs.layout.summary(root)
 }

 // Clear deletes all files on the filesystem.
@@ -316,36 +304,3 @@ func (bs *BlobStorage) WithinRetentionPeriod(requested, current primitives.Epoch
 	}
 	return requested+bs.retentionEpochs >= current
 }
-
-type blobNamer struct {
-	root  [32]byte
-	index uint64
-}
-
-func namerForSidecar(sc blocks.VerifiedROBlob) blobNamer {
-	return blobNamer{root: sc.BlockRoot(), index: sc.Index}
-}
-
-func (p blobNamer) dir() string {
-	return rootString(p.root)
-}
-
-func (p blobNamer) partPath(entropy string) string {
-	return path.Join(p.dir(), fmt.Sprintf("%s-%d.%s", entropy, p.index, partExt))
-}
-
-func (p blobNamer) path() string {
-	return path.Join(p.dir(), fmt.Sprintf("%d.%s", p.index, sszExt))
-}
-
-func rootString(root [32]byte) string {
-	return fmt.Sprintf("%#x", root)
-}
-
-func stringToRoot(str string) ([32]byte, error) {
-	slice, err := hexutil.Decode(str)
-	if err != nil {
-		return [32]byte{}, errors.Wrapf(errInvalidRootString, "input=%s", str)
-	}
-	return bytesutil.ToBytes32(slice), nil
-}
--- a/beacon-chain/db/filesystem/blob_test.go
+++ b/beacon-chain/db/filesystem/blob_test.go
@@ -9,26 +9,26 @@ import (
 	"testing"

 	ssz "github.com/prysmaticlabs/fastssz"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/verification"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
-	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
 	"github.com/spf13/afero"
 )

 func TestBlobStorage_SaveBlobData(t *testing.T) {
 	_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, 1, params.BeaconConfig().MaxBlobsPerBlock(1))
-	testSidecars, err := verification.BlobSidecarSliceNoop(sidecars)
-	require.NoError(t, err)
+	testSidecars := verification.FakeVerifySliceForTest(t, sidecars)

 	t.Run("no error for duplicate", func(t *testing.T) {
-		fs, bs := NewEphemeralBlobStorageWithFs(t)
+		fs, bs := NewEphemeralBlobStorageAndFs(t)
 		existingSidecar := testSidecars[0]

-		blobPath := namerForSidecar(existingSidecar).path()
+		blobPath := bs.layout.sszPath(identForSidecar(existingSidecar))
 		// Serialize the existing BlobSidecar to binary data.
 		existingSidecarData, err := ssz.MarshalSSZ(existingSidecar)
 		require.NoError(t, err)
@@ -56,8 +56,8 @@ func TestBlobStorage_SaveBlobData(t *testing.T) {
 		require.NoError(t, bs.Save(sc))
 		actualSc, err := bs.Get(sc.BlockRoot(), sc.Index)
 		require.NoError(t, err)
-		expectedIdx := []bool{false, false, true, false, false, false}
-		actualIdx, err := bs.Indices(actualSc.BlockRoot(), 100)
+		expectedIdx := blobIndexMask{false, false, true, false, false, false}
+		actualIdx := bs.Summary(actualSc.BlockRoot()).mask
 		require.NoError(t, err)
 		require.DeepEqual(t, expectedIdx, actualIdx)
 	})
@@ -85,7 +85,7 @@ func TestBlobStorage_SaveBlobData(t *testing.T) {

 		require.NoError(t, bs.Remove(expected.BlockRoot()))
 		_, err = bs.Get(expected.BlockRoot(), expected.Index)
-		require.ErrorContains(t, "file does not exist", err)
+		require.Equal(t, true, db.IsNotFound(err))
 	})

 	t.Run("clear", func(t *testing.T) {
@@ -126,16 +126,14 @@ func TestBlobStorage_SaveBlobData(t *testing.T) {
 	})
 }

-// pollUntil polls a condition function until it returns true or a timeout is reached.
-
 func TestBlobIndicesBounds(t *testing.T) {
-	fs, bs := NewEphemeralBlobStorageWithFs(t)
+	fs := afero.NewMemMapFs()
 	root := [32]byte{}

 	okIdx := uint64(params.BeaconConfig().MaxBlobsPerBlock(0)) - 1
-	writeFakeSSZ(t, fs, root, okIdx)
-	indices, err := bs.Indices(root, 100)
-	require.NoError(t, err)
+	writeFakeSSZ(t, fs, root, 0, okIdx)
+	bs := NewWarmedEphemeralBlobStorageUsingFs(t, fs, WithLayout(LayoutNameByEpoch))
+	indices := bs.Summary(root).mask
 	expected := make([]bool, params.BeaconConfig().MaxBlobsPerBlock(0))
 	expected[okIdx] = true
 	for i := range expected {
@@ -143,102 +141,23 @@ func TestBlobIndicesBounds(t *testing.T) {
 	}

 	oobIdx := uint64(params.BeaconConfig().MaxBlobsPerBlock(0))
-	writeFakeSSZ(t, fs, root, oobIdx)
-	_, err = bs.Indices(root, 100)
-	require.ErrorIs(t, err, errIndexOutOfBounds)
+	writeFakeSSZ(t, fs, root, 0, oobIdx)
+	// This now fails at cache warmup time.
+	require.ErrorIs(t, warmCache(bs.layout, bs.cache), errIndexOutOfBounds)
 }

-func writeFakeSSZ(t *testing.T, fs afero.Fs, root [32]byte, idx uint64) {
-	namer := blobNamer{root: root, index: idx}
-	require.NoError(t, fs.MkdirAll(namer.dir(), 0700))
-	fh, err := fs.Create(namer.path())
+func writeFakeSSZ(t *testing.T, fs afero.Fs, root [32]byte, slot primitives.Slot, idx uint64) {
+	epoch := slots.ToEpoch(slot)
+	namer := newBlobIdent(root, epoch, idx)
+	layout := periodicEpochLayout{}
+	require.NoError(t, fs.MkdirAll(layout.dir(namer), 0700))
+	fh, err := fs.Create(layout.sszPath(namer))
 	require.NoError(t, err)
 	_, err = fh.Write([]byte("derp"))
 	require.NoError(t, err)
 	require.NoError(t, fh.Close())
 }

-func TestBlobStoragePrune(t *testing.T) {
-	currentSlot := primitives.Slot(200000)
-	fs, bs := NewEphemeralBlobStorageWithFs(t)
-
-	t.Run("PruneOne", func(t *testing.T) {
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, 300, params.BeaconConfig().MaxBlobsPerBlock(0))
-		testSidecars, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-
-		for _, sidecar := range testSidecars {
-			require.NoError(t, bs.Save(sidecar))
-		}
-
-		require.NoError(t, bs.pruner.prune(currentSlot-bs.pruner.windowSize))
-
-		remainingFolders, err := afero.ReadDir(fs, ".")
-		require.NoError(t, err)
-		require.Equal(t, 0, len(remainingFolders))
-	})
-	t.Run("Prune dangling blob", func(t *testing.T) {
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, 299, params.BeaconConfig().MaxBlobsPerBlock(0))
-		testSidecars, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-
-		for _, sidecar := range testSidecars[4:] {
-			require.NoError(t, bs.Save(sidecar))
-		}
-
-		require.NoError(t, bs.pruner.prune(currentSlot-bs.pruner.windowSize))
-
-		remainingFolders, err := afero.ReadDir(fs, ".")
-		require.NoError(t, err)
-		require.Equal(t, 0, len(remainingFolders))
-	})
-	t.Run("PruneMany", func(t *testing.T) {
-		blockQty := 10
-		slot := primitives.Slot(1)
-
-		for j := 0; j <= blockQty; j++ {
-			root := bytesutil.ToBytes32(bytesutil.ToBytes(uint64(slot), 32))
-			_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, root, slot, params.BeaconConfig().MaxBlobsPerBlock(0))
-			testSidecars, err := verification.BlobSidecarSliceNoop(sidecars)
-			require.NoError(t, err)
-			require.NoError(t, bs.Save(testSidecars[0]))
-
-			slot += 10000
-		}
-
-		require.NoError(t, bs.pruner.prune(currentSlot-bs.pruner.windowSize))
-
-		remainingFolders, err := afero.ReadDir(fs, ".")
-		require.NoError(t, err)
-		require.Equal(t, 4, len(remainingFolders))
-	})
-}
-
-func BenchmarkPruning(b *testing.B) {
-	var t *testing.T
-	_, bs := NewEphemeralBlobStorageWithFs(t)
-
-	blockQty := 10000
-	currentSlot := primitives.Slot(150000)
-	slot := primitives.Slot(0)
-
-	for j := 0; j <= blockQty; j++ {
-		root := bytesutil.ToBytes32(bytesutil.ToBytes(uint64(slot), 32))
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, root, slot, params.BeaconConfig().MaxBlobsPerBlock(0))
-		testSidecars, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-		require.NoError(t, bs.Save(testSidecars[0]))
-
-		slot += 100
-	}
-	b.ReportAllocs()
-	b.ResetTimer()
-	for i := 0; i < b.N; i++ {
-		err := bs.pruner.prune(currentSlot)
-		require.NoError(b, err)
-	}
-}
-
 func TestNewBlobStorage(t *testing.T) {
 	_, err := NewBlobStorage()
 	require.ErrorIs(t, err, errNoBasePath)
@@ -292,3 +211,13 @@ func TestConfig_WithinRetentionPeriod(t *testing.T) {
 		require.Equal(t, true, storage.WithinRetentionPeriod(1, 1))
 	})
 }
+
+func TestLayoutNames(t *testing.T) {
+	badLayoutName := "bad"
+	for _, name := range LayoutNames {
+		_, err := newLayout(name, nil, nil, nil)
+		require.NoError(t, err)
+	}
+	_, err := newLayout(badLayoutName, nil, nil, nil)
+	require.ErrorIs(t, err, errInvalidLayoutName)
+}
--- a/beacon-chain/db/filesystem/cache.go
+++ b/beacon-chain/db/filesystem/cache.go
@@ -1,8 +1,10 @@
 package filesystem

 import (
+	"fmt"
 	"sync"

+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db"
 	fieldparams "github.com/prysmaticlabs/prysm/v5/config/fieldparams"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
@@ -13,17 +15,12 @@ type blobIndexMask []bool

 // BlobStorageSummary represents cached information about the BlobSidecars on disk for each root the cache knows about.
 type BlobStorageSummary struct {
-	slot primitives.Slot
-	mask blobIndexMask
+	epoch primitives.Epoch
+	mask  blobIndexMask
 }

 // HasIndex returns true if the BlobSidecar at the given index is available in the filesystem.
 func (s BlobStorageSummary) HasIndex(idx uint64) bool {
-	// Protect from panic, but assume callers are sophisticated enough to not need an error telling them they have an invalid idx.
-	maxBlobsPerBlock := params.BeaconConfig().MaxBlobsPerBlock(s.slot)
-	if idx >= uint64(maxBlobsPerBlock) {
-		return false
-	}
 	if idx >= uint64(len(s.mask)) {
 		return false
 	}
@@ -32,10 +29,6 @@ func (s BlobStorageSummary) HasIndex(idx uint64) bool {

 // AllAvailable returns true if we have all blobs for all indices from 0 to count-1.
 func (s BlobStorageSummary) AllAvailable(count int) bool {
-	maxBlobsPerBlock := params.BeaconConfig().MaxBlobsPerBlock(s.slot)
-	if count > maxBlobsPerBlock {
-		return false
-	}
 	if count > len(s.mask) {
 		return false
 	}
@@ -47,83 +40,121 @@ func (s BlobStorageSummary) AllAvailable(count int) bool {
 	return true
 }

+func (s BlobStorageSummary) MaxBlobsForEpoch() uint64 {
+	return uint64(params.BeaconConfig().MaxBlobsPerBlockAtEpoch(s.epoch))
+}
+
+// NewBlobStorageSummary creates a new BlobStorageSummary for a given epoch and mask.
+func NewBlobStorageSummary(epoch primitives.Epoch, mask []bool) (BlobStorageSummary, error) {
+	c := params.BeaconConfig().MaxBlobsPerBlockAtEpoch(epoch)
+	if len(mask) != c {
+		return BlobStorageSummary{}, fmt.Errorf("mask length %d does not match expected %d for epoch %d", len(mask), c, epoch)
+	}
+	return BlobStorageSummary{
+		epoch: epoch,
+		mask:  mask,
+	}, nil
+}
+
 // BlobStorageSummarizer can be used to receive a summary of metadata about blobs on disk for a given root.
 // The BlobStorageSummary can be used to check which indices (if any) are available for a given block by root.
 type BlobStorageSummarizer interface {
 	Summary(root [32]byte) BlobStorageSummary
 }

-type blobStorageCache struct {
+type blobStorageSummaryCache struct {
 	mu     sync.RWMutex
 	nBlobs float64
 	cache  map[[32]byte]BlobStorageSummary
 }

-var _ BlobStorageSummarizer = &blobStorageCache{}
+var _ BlobStorageSummarizer = &blobStorageSummaryCache{}

-func newBlobStorageCache() *blobStorageCache {
-	return &blobStorageCache{
-		cache: make(map[[32]byte]BlobStorageSummary, params.BeaconConfig().MinEpochsForBlobsSidecarsRequest*fieldparams.SlotsPerEpoch),
+func newBlobStorageCache() *blobStorageSummaryCache {
+	return &blobStorageSummaryCache{
+		cache: make(map[[32]byte]BlobStorageSummary),
 	}
 }

 // Summary returns the BlobStorageSummary for `root`. The BlobStorageSummary can be used to check for the presence of
 // BlobSidecars based on Index.
-func (s *blobStorageCache) Summary(root [32]byte) BlobStorageSummary {
+func (s *blobStorageSummaryCache) Summary(root [32]byte) BlobStorageSummary {
 	s.mu.RLock()
 	defer s.mu.RUnlock()
 	return s.cache[root]
 }

-func (s *blobStorageCache) ensure(key [32]byte, slot primitives.Slot, idx uint64) error {
-	maxBlobsPerBlock := params.BeaconConfig().MaxBlobsPerBlock(slot)
-	if idx >= uint64(maxBlobsPerBlock) {
+func (s *blobStorageSummaryCache) ensure(ident blobIdent) error {
+	maxBlobsPerBlock := params.BeaconConfig().MaxBlobsPerBlockAtEpoch(ident.epoch)
+	if ident.index >= uint64(maxBlobsPerBlock) {
 		return errIndexOutOfBounds
 	}
 	s.mu.Lock()
 	defer s.mu.Unlock()
-	v := s.cache[key]
-	v.slot = slot
+	v := s.cache[ident.root]
+	v.epoch = ident.epoch
 	if v.mask == nil {
 		v.mask = make(blobIndexMask, maxBlobsPerBlock)
 	}
-	if !v.mask[idx] {
+	if !v.mask[ident.index] {
 		s.updateMetrics(1)
 	}
-	v.mask[idx] = true
-	s.cache[key] = v
+	v.mask[ident.index] = true
+	s.cache[ident.root] = v
 	return nil
 }

-func (s *blobStorageCache) slot(key [32]byte) (primitives.Slot, bool) {
+func (s *blobStorageSummaryCache) get(key [32]byte) (BlobStorageSummary, bool) {
 	s.mu.RLock()
 	defer s.mu.RUnlock()
 	v, ok := s.cache[key]
-	if !ok {
-		return 0, false
-	}
-	return v.slot, ok
+	return v, ok
 }

-func (s *blobStorageCache) evict(key [32]byte) {
-	var deleted float64
+func (s *blobStorageSummaryCache) identForIdx(key [32]byte, idx uint64) (blobIdent, error) {
+	v, ok := s.get(key)
+	if !ok || !v.HasIndex(idx) {
+		return blobIdent{}, db.ErrNotFound
+	}
+	return blobIdent{
+		root:  key,
+		index: idx,
+		epoch: v.epoch,
+	}, nil
+}
+
+func (s *blobStorageSummaryCache) identForRoot(key [32]byte) (blobIdent, error) {
+	v, ok := s.get(key)
+	if !ok {
+		return blobIdent{}, db.ErrNotFound
+	}
+	return blobIdent{
+		root:  key,
+		epoch: v.epoch,
+	}, nil
+}
+
+func (s *blobStorageSummaryCache) evict(key [32]byte) int {
+	deleted := 0
 	s.mu.Lock()
+	defer s.mu.Unlock()
 	v, ok := s.cache[key]
-	if ok {
-		for i := range v.mask {
-			if v.mask[i] {
-				deleted += 1
-			}
+	if !ok {
+		return 0
+	}
+	for i := range v.mask {
+		if v.mask[i] {
+			deleted += 1
 		}
 	}
 	delete(s.cache, key)
-	s.mu.Unlock()
 	if deleted > 0 {
-		s.updateMetrics(-deleted)
+		s.updateMetrics(-float64(deleted))
 	}
+	return deleted
 }

-func (s *blobStorageCache) updateMetrics(delta float64) {
+func (s *blobStorageSummaryCache) updateMetrics(delta float64) {
 	s.nBlobs += delta
 	blobDiskCount.Set(s.nBlobs)
 	blobDiskSize.Set(s.nBlobs * fieldparams.BlobSidecarSize)
--- a/beacon-chain/db/filesystem/cache_test.go
+++ b/beacon-chain/db/filesystem/cache_test.go
@@ -53,7 +53,7 @@ func TestSlotByRoot_Summary(t *testing.T) {
 	for _, c := range cases {
 		if c.expected != nil {
 			key := bytesutil.ToBytes32([]byte(c.name))
-			sc.cache[key] = BlobStorageSummary{slot: 0, mask: c.expected}
+			sc.cache[key] = BlobStorageSummary{epoch: 0, mask: c.expected}
 		}
 	}
 	for _, c := range cases {
--- a/beacon-chain/db/filesystem/iteration.go
+++ b/beacon-chain/db/filesystem/iteration.go
@@ -0,0 +1,238 @@
+package filesystem
+
+import (
+	"fmt"
+	"io"
+	"path"
+	"path/filepath"
+	"strconv"
+	"strings"
+
+	"github.com/ethereum/go-ethereum/common/hexutil"
+	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
+	"github.com/sirupsen/logrus"
+	"github.com/spf13/afero"
+)
+
+var errIdentFailure = errors.New("failed to determine blob metadata, ignoring all sub-paths.")
+
+type identificationError struct {
+	err   error
+	path  string
+	ident blobIdent
+}
+
+func (ide *identificationError) Error() string {
+	return fmt.Sprintf("%s path=%s, err=%s", errIdentFailure.Error(), ide.path, ide.err.Error())
+}
+
+func (ide *identificationError) Unwrap() error {
+	return ide.err
+}
+
+func (*identificationError) Is(err error) bool {
+	return err == errIdentFailure
+}
+
+func (ide *identificationError) LogFields() logrus.Fields {
+	fields := ide.ident.logFields()
+	fields["path"] = ide.path
+	return fields
+}
+
+func newIdentificationError(path string, ident blobIdent, err error) *identificationError {
+	return &identificationError{path: path, ident: ident, err: err}
+}
+
+func listDir(fs afero.Fs, dir string) ([]string, error) {
+	top, err := fs.Open(dir)
+	if err != nil {
+		return nil, errors.Wrap(err, "failed to open directory descriptor")
+	}
+	defer func() {
+		if err := top.Close(); err != nil {
+			log.WithError(err).Errorf("Could not close file %s", dir)
+		}
+	}()
+	// re the -1 param: "If n <= 0, Readdirnames returns all the names from the directory in a single slice"
+	dirs, err := top.Readdirnames(-1)
+	if err != nil {
+		return nil, errors.Wrap(err, "failed to read directory listing")
+	}
+	return dirs, nil
+}
+
+// identPopulator is a function that sets values in the blobIdent for a given layer of the filesystem layout.
+type identPopulator func(blobIdent, string) (blobIdent, error)
+
+// layoutLayer represents a layer of the nested directory scheme. Each layer is defined by a filter function that
+// ensures any entries at that layer of the scheme are named in a valid way, and a populateIdent function that
+// parses the directory name into a blobIdent object, used for iterating across the layout in a layout-independent way.
+type layoutLayer struct {
+	populateIdent identPopulator
+	filter        func(string) bool
+}
+
+// identIterator moves through the filesystem in order to yield blobIdents.
+// layoutLayers (in the 'layers' field) allows a filesystem layout to control how the
+// layout is traversed. A layoutLayer can filter out entries from the directory listing
+// via the filter function, and populate fields in the blobIdent via the populateIdent function.
+// The blobIdent is populated from an empty value at the root, accumulating values for its fields at each layer.
+// The fully populated blobIdent is returned when the iterator reaches the leaf layer.
+type identIterator struct {
+	fs    afero.Fs
+	path  string
+	child *identIterator
+	ident blobIdent
+	// layoutLayers are the heart of how the layout defines the nesting of the components of the path.
+	// Each layer of the layout represents a different layer of the directory layout hierarchy,
+	// from the relative root at the zero index to the blob files at the end.
+	layers  []layoutLayer
+	entries []string
+	offset  int
+	eof     bool
+}
+
+// atEOF can be used to peek at the iterator to see if it's already finished. This is useful for the migration code to check
+// if there are any entries in the directory indicated by the migration.
+func (iter *identIterator) atEOF() bool {
+	return iter.eof
+}
+
+// next is the only method that a user of the identIterator needs to call.
+// identIterator will yield blobIdents in a breadth-first fashion,
+// returning an empty blobIdent and io.EOF once all branches have been traversed.
+func (iter *identIterator) next() (blobIdent, error) {
+	if iter.eof {
+		return blobIdent{}, io.EOF
+	}
+	if iter.child != nil {
+		next, err := iter.child.next()
+		if err == nil {
+			return next, nil
+		}
+		if !errors.Is(err, io.EOF) {
+			return blobIdent{}, err
+		}
+	}
+	return iter.advanceChild()
+}
+
+// advanceChild is used to move to the next directory at each layer of the tree, either when
+// the nodes are first being initialized at a layer, or when a sub-branch has been exhausted.
+func (iter *identIterator) advanceChild() (blobIdent, error) {
+	defer func() {
+		iter.offset += 1
+	}()
+	for i := iter.offset; i < len(iter.entries); i++ {
+		iter.offset = i
+		nextPath := filepath.Join(iter.path, iter.entries[iter.offset])
+		nextLayer := iter.layers[0]
+		if !nextLayer.filter(nextPath) {
+			continue
+		}
+		ident, err := nextLayer.populateIdent(iter.ident, nextPath)
+		if err != nil {
+			return ident, newIdentificationError(nextPath, ident, err)
+		}
+		// if we're at the leaf layer , we can return the updated ident.
+		if len(iter.layers) == 1 {
+			return ident, nil
+		}
+
+		entries, err := listDir(iter.fs, nextPath)
+		if err != nil {
+			return blobIdent{}, err
+		}
+		if len(entries) == 0 {
+			continue
+		}
+		iter.child = &identIterator{
+			fs:      iter.fs,
+			path:    nextPath,
+			ident:   ident,
+			layers:  iter.layers[1:],
+			entries: entries,
+		}
+		return iter.child.next()
+	}
+
+	return blobIdent{}, io.EOF
+}
+
+func populateNoop(namer blobIdent, _ string) (blobIdent, error) {
+	return namer, nil
+}
+
+func populateRoot(namer blobIdent, dir string) (blobIdent, error) {
+	root, err := rootFromPath(dir)
+	if err != nil {
+		return namer, err
+	}
+	namer.root = root
+	return namer, nil
+}
+
+func populateIndex(namer blobIdent, fname string) (blobIdent, error) {
+	idx, err := idxFromPath(fname)
+	if err != nil {
+		return namer, err
+	}
+	namer.index = idx
+	return namer, nil
+}
+
+func rootFromPath(p string) ([32]byte, error) {
+	subdir := filepath.Base(p)
+	root, err := stringToRoot(subdir)
+	if err != nil {
+		return root, errors.Wrapf(err, "invalid directory, could not parse subdir as root %s", p)
+	}
+	return root, nil
+}
+
+func idxFromPath(p string) (uint64, error) {
+	p = path.Base(p)
+
+	if !isSszFile(p) {
+		return 0, errors.Wrap(errNotBlobSSZ, "does not have .ssz extension")
+	}
+	parts := strings.Split(p, ".")
+	if len(parts) != 2 {
+		return 0, errors.Wrap(errNotBlobSSZ, "unexpected filename structure (want <index>.ssz)")
+	}
+	idx, err := strconv.ParseUint(parts[0], 10, 64)
+	if err != nil {
+		return 0, err
+	}
+	return idx, nil
+}
+
+func filterNoop(_ string) bool {
+	return true
+}
+
+func isRootDir(p string) bool {
+	dir := filepath.Base(p)
+	return len(dir) == rootStringLen && strings.HasPrefix(dir, "0x")
+}
+
+func isSszFile(s string) bool {
+	return filepath.Ext(s) == "."+sszExt
+}
+
+func rootToString(root [32]byte) string {
+	return fmt.Sprintf("%#x", root)
+}
+
+func stringToRoot(str string) ([32]byte, error) {
+	if len(str) != rootStringLen {
+		return [32]byte{}, errors.Wrapf(errInvalidRootString, "incorrect len for input=%s", str)
+	}
+	slice, err := hexutil.Decode(str)
+	if err != nil {
+		return [32]byte{}, errors.Wrapf(errInvalidRootString, "input=%s", str)
+	}
+	return bytesutil.ToBytes32(slice), nil
+}
--- a/beacon-chain/db/filesystem/iteration_test.go
+++ b/beacon-chain/db/filesystem/iteration_test.go
@@ -0,0 +1,304 @@
+package filesystem
+
+import (
+	"bytes"
+	"fmt"
+	"io"
+	"math"
+	"os"
+	"path"
+	"sort"
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/verification"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	"github.com/spf13/afero"
+)
+
+func TestRootFromDir(t *testing.T) {
+	cases := []struct {
+		name string
+		dir  string
+		err  error
+		root [32]byte
+	}{
+		{
+			name: "happy path",
+			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cb",
+			root: [32]byte{255, 255, 135, 94, 29, 152, 92, 92, 203, 33, 72, 148, 152, 63, 36, 40,
+				237, 178, 113, 240, 248, 123, 104, 186, 112, 16, 228, 169, 157, 243, 181, 203},
+		},
+		{
+			name: "too short",
+			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5c",
+			err:  errInvalidRootString,
+		},
+		{
+			name: "too log",
+			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cbb",
+			err:  errInvalidRootString,
+		},
+		{
+			name: "missing prefix",
+			dir:  "ffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cb",
+			err:  errInvalidRootString,
+		},
+	}
+	for _, c := range cases {
+		t.Run(c.name, func(t *testing.T) {
+			root, err := stringToRoot(c.dir)
+			if c.err != nil {
+				require.ErrorIs(t, err, c.err)
+				return
+			}
+			require.NoError(t, err)
+			require.Equal(t, c.root, root)
+		})
+	}
+}
+
+func TestSlotFromFile(t *testing.T) {
+	cases := []struct {
+		slot primitives.Slot
+	}{
+		{slot: 0},
+		{slot: 2},
+		{slot: 1123581321},
+		{slot: math.MaxUint64},
+	}
+	for _, c := range cases {
+		t.Run(fmt.Sprintf("slot %d", c.slot), func(t *testing.T) {
+			fs, bs := NewEphemeralBlobStorageAndFs(t)
+			_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, c.slot, 1)
+			sc := verification.FakeVerifyForTest(t, sidecars[0])
+			require.NoError(t, bs.Save(sc))
+			namer := identForSidecar(sc)
+			sszPath := bs.layout.sszPath(namer)
+			slot, err := slotFromFile(sszPath, fs)
+			require.NoError(t, err)
+			require.Equal(t, c.slot, slot)
+		})
+	}
+}
+
+type dirFiles struct {
+	name     string
+	isDir    bool
+	children []dirFiles
+}
+
+func (df dirFiles) reify(t *testing.T, fs afero.Fs, base string) {
+	fullPath := path.Join(base, df.name)
+	if df.isDir {
+		if df.name != "" {
+			require.NoError(t, fs.Mkdir(fullPath, directoryPermissions()))
+		}
+		for _, c := range df.children {
+			c.reify(t, fs, fullPath)
+		}
+	} else {
+		fp, err := fs.Create(fullPath)
+		require.NoError(t, err)
+		_, err = fp.WriteString("derp")
+		require.NoError(t, err)
+	}
+}
+
+func (df dirFiles) childNames() []string {
+	cn := make([]string, len(df.children))
+	for i := range df.children {
+		cn[i] = df.children[i].name
+	}
+	return cn
+}
+
+func TestListDir(t *testing.T) {
+	fs := afero.NewMemMapFs()
+	rootStrs := []string{
+		"0x0023dc5d063c7c1b37016bb54963c6ff4bfe5dfdf6dac29e7ceeb2b8fa81ed7a",
+		"0xff30526cd634a5af3a09cc9bff67f33a621fc5b975750bb4432f74df077554b4",
+		"0x23f5f795aaeb78c01fadaf3d06da2e99bd4b3622ae4dfea61b05b7d9adb119c2",
+	}
+
+	// parent directory
+	tree := dirFiles{isDir: true}
+	// break out each subdir for easier assertions
+	notABlob := dirFiles{name: "notABlob", isDir: true}
+	childlessBlob := dirFiles{name: rootStrs[0], isDir: true}
+	blobWithSsz := dirFiles{name: rootStrs[1], isDir: true,
+		children: []dirFiles{{name: "1.ssz"}, {name: "2.ssz"}},
+	}
+	blobWithSszAndTmp := dirFiles{name: rootStrs[2], isDir: true,
+		children: []dirFiles{{name: "5.ssz"}, {name: "0.part"}}}
+	tree.children = append(tree.children,
+		notABlob, childlessBlob, blobWithSsz, blobWithSszAndTmp)
+
+	topChildren := make([]string, len(tree.children))
+	for i := range tree.children {
+		topChildren[i] = tree.children[i].name
+	}
+
+	var filter = func(entries []string, filt func(string) bool) []string {
+		filtered := make([]string, 0, len(entries))
+		for i := range entries {
+			if filt(entries[i]) {
+				filtered = append(filtered, entries[i])
+			}
+		}
+		return filtered
+	}
+
+	tree.reify(t, fs, "")
+	cases := []struct {
+		name     string
+		dirPath  string
+		expected []string
+		filter   func(string) bool
+		err      error
+	}{
+		{
+			name:     "non-existent",
+			dirPath:  "derp",
+			expected: []string{},
+			err:      os.ErrNotExist,
+		},
+		{
+			name:     "empty",
+			dirPath:  childlessBlob.name,
+			expected: []string{},
+		},
+		{
+			name:     "top",
+			dirPath:  ".",
+			expected: topChildren,
+		},
+		{
+			name:     "custom filter: only notABlob",
+			dirPath:  ".",
+			expected: []string{notABlob.name},
+			filter: func(s string) bool {
+				return s == notABlob.name
+			},
+		},
+		{
+			name:     "root filter",
+			dirPath:  ".",
+			expected: []string{childlessBlob.name, blobWithSsz.name, blobWithSszAndTmp.name},
+			filter:   isRootDir,
+		},
+		{
+			name:     "ssz filter",
+			dirPath:  blobWithSsz.name,
+			expected: blobWithSsz.childNames(),
+			filter:   isSszFile,
+		},
+		{
+			name:     "ssz mixed filter",
+			dirPath:  blobWithSszAndTmp.name,
+			expected: []string{"5.ssz"},
+			filter:   isSszFile,
+		},
+	}
+	for _, c := range cases {
+		t.Run(c.name, func(t *testing.T) {
+			result, err := listDir(fs, c.dirPath)
+			if c.filter != nil {
+				result = filter(result, c.filter)
+			}
+			if c.err != nil {
+				require.ErrorIs(t, err, c.err)
+				require.Equal(t, 0, len(result))
+			} else {
+				require.NoError(t, err)
+				sort.Strings(c.expected)
+				sort.Strings(result)
+				require.DeepEqual(t, c.expected, result)
+			}
+		})
+	}
+}
+
+func TestSlotFromBlob(t *testing.T) {
+	cases := []struct {
+		slot primitives.Slot
+	}{
+		{slot: 0},
+		{slot: 2},
+		{slot: 1123581321},
+		{slot: math.MaxUint64},
+	}
+	for _, c := range cases {
+		t.Run(fmt.Sprintf("slot %d", c.slot), func(t *testing.T) {
+			_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, c.slot, 1)
+			sc := sidecars[0]
+			enc, err := sc.MarshalSSZ()
+			require.NoError(t, err)
+			slot, err := slotFromBlob(bytes.NewReader(enc))
+			require.NoError(t, err)
+			require.Equal(t, c.slot, slot)
+		})
+	}
+}
+
+func TestIterationComplete(t *testing.T) {
+	targets := []migrationTestTarget{
+		{
+			ident: ezIdent(t, "0x0125e54c64c925018c9296965a5b622d9f5ab626c10917860dcfb6aa09a0a00b", 1234, 0),
+			path:  "by-epoch/0/1234/0x0125e54c64c925018c9296965a5b622d9f5ab626c10917860dcfb6aa09a0a00b/0.ssz",
+		},
+		{
+			ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 0),
+			slotOffset: 31,
+			path:       "by-epoch/1/5330/0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86/0.ssz",
+		},
+		{
+			ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 1),
+			slotOffset: 31,
+			path:       "by-epoch/1/5330/0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86/1.ssz",
+		},
+		{
+			ident:      ezIdent(t, "0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c", 16777216, 0),
+			slotOffset: 16,
+			path:       "by-epoch/4096/16777216/0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c/0.ssz",
+		},
+		{
+			ident:      ezIdent(t, "0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c", 16777216, 1),
+			slotOffset: 16,
+			path:       "by-epoch/4096/16777216/0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c/1.ssz",
+		},
+		{
+			ident:      ezIdent(t, "0x42eabe3d2c125410cd226de6f2825fb7575ab896c3f52e43de1fa29e4c809aba", 16777217, 0),
+			slotOffset: 16,
+			path:       "by-epoch/4096/16777217/0x42eabe3d2c125410cd226de6f2825fb7575ab896c3f52e43de1fa29e4c809aba/0.ssz",
+		},
+		{
+			ident: ezIdent(t, "0x666cea5034e22bd3b849cb33914cad59afd88ee08e4d5bc0e997411c945fbc1d", 11235, 1),
+			path:  "by-epoch/2/11235/0x666cea5034e22bd3b849cb33914cad59afd88ee08e4d5bc0e997411c945fbc1d/1.ssz",
+		},
+	}
+	fs := afero.NewMemMapFs()
+	cache := newBlobStorageCache()
+	byEpoch, err := newLayout(LayoutNameByEpoch, fs, cache, nil)
+	require.NoError(t, err)
+	for _, tar := range targets {
+		setupTestBlobFile(t, tar.ident, tar.slotOffset, fs, byEpoch)
+	}
+	iter, err := byEpoch.iterateIdents(0)
+	require.NoError(t, err)
+	nIdents := 0
+	for ident, err := iter.next(); err != io.EOF; ident, err = iter.next() {
+		require.NoError(t, err)
+		nIdents++
+		require.NoError(t, cache.ensure(ident))
+	}
+	require.Equal(t, len(targets), nIdents)
+	for _, tar := range targets {
+		entry, ok := cache.get(tar.ident.root)
+		require.Equal(t, true, ok)
+		require.Equal(t, tar.ident.epoch, entry.epoch)
+		require.Equal(t, true, entry.HasIndex(tar.ident.index))
+		require.Equal(t, tar.path, byEpoch.sszPath(tar.ident))
+	}
+}
--- a/beacon-chain/db/filesystem/layout.go
+++ b/beacon-chain/db/filesystem/layout.go
@@ -0,0 +1,291 @@
+package filesystem
+
+import (
+	"fmt"
+	"io"
+	"path/filepath"
+	"strings"
+	"time"
+
+	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/config/params"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
+	"github.com/sirupsen/logrus"
+	"github.com/spf13/afero"
+)
+
+const (
+	// Full root in directory will be 66 chars, eg:
+	// >>> len('0x0002fb4db510b8618b04dc82d023793739c26346a8b02eb73482e24b0fec0555') == 66
+	rootStringLen        = 66
+	sszExt               = "ssz"
+	partExt              = "part"
+	periodicEpochBaseDir = "by-epoch"
+)
+
+const (
+	LayoutNameFlat    = "flat"
+	LayoutNameByEpoch = "by-epoch"
+)
+
+var LayoutNames = []string{LayoutNameFlat, LayoutNameByEpoch}
+
+var (
+	errMigrationFailure       = errors.New("unable to migrate blob directory between old and new layout")
+	errCacheWarmFailed        = errors.New("failed to warm blob filesystem cache")
+	errPruneFailed            = errors.New("failed to prune root")
+	errInvalidRootString      = errors.New("Could not parse hex string as a [32]byte")
+	errInvalidDirectoryLayout = errors.New("Could not parse blob directory path")
+	errInvalidLayoutName      = errors.New("unknown layout name")
+	errLayoutNotDetected      = errors.New("given layout not observed in the blob filesystem tree")
+)
+
+type blobIdent struct {
+	root  [32]byte
+	epoch primitives.Epoch
+	index uint64
+}
+
+func newBlobIdent(root [32]byte, epoch primitives.Epoch, index uint64) blobIdent {
+	return blobIdent{root: root, epoch: epoch, index: index}
+}
+
+func identForSidecar(sc blocks.VerifiedROBlob) blobIdent {
+	return newBlobIdent(sc.BlockRoot(), slots.ToEpoch(sc.Slot()), sc.Index)
+}
+
+func (n blobIdent) sszFname() string {
+	return fmt.Sprintf("%d.%s", n.index, sszExt)
+}
+
+func (n blobIdent) partFname(entropy string) string {
+	return fmt.Sprintf("%s-%d.%s", entropy, n.index, partExt)
+}
+
+func (n blobIdent) logFields() logrus.Fields {
+	return logrus.Fields{
+		"root":  fmt.Sprintf("%#x", n.root),
+		"epoch": n.epoch,
+		"index": n.index,
+	}
+}
+
+type fsLayout interface {
+	name() string
+	dir(n blobIdent) string
+	sszPath(n blobIdent) string
+	partPath(n blobIdent, entropy string) string
+	iterateIdents(before primitives.Epoch) (*identIterator, error)
+	ident(root [32]byte, idx uint64) (blobIdent, error)
+	dirIdent(root [32]byte) (blobIdent, error)
+	summary(root [32]byte) BlobStorageSummary
+	notify(ident blobIdent) error
+	pruneBefore(before primitives.Epoch) (*pruneSummary, error)
+	remove(ident blobIdent) (int, error)
+	blockParentDirs(ident blobIdent) []string
+}
+
+func newLayout(name string, fs afero.Fs, cache *blobStorageSummaryCache, pruner *blobPruner) (fsLayout, error) {
+	switch name {
+	case LayoutNameFlat:
+		return newFlatLayout(fs, cache, pruner), nil
+	case LayoutNameByEpoch:
+		return newPeriodicEpochLayout(fs, cache, pruner), nil
+	default:
+		return nil, errors.Wrapf(errInvalidLayoutName, "name=%s", name)
+	}
+}
+
+func warmCache(l fsLayout, cache *blobStorageSummaryCache) error {
+	iter, err := l.iterateIdents(0)
+	if err != nil {
+		return errors.Wrap(errCacheWarmFailed, err.Error())
+	}
+	for ident, err := iter.next(); !errors.Is(err, io.EOF); ident, err = iter.next() {
+		if errors.Is(err, errIdentFailure) {
+			idf := &identificationError{}
+			if errors.As(err, &idf) {
+				log.WithFields(idf.LogFields()).WithError(err).Error("Failed to cache blob data for path")
+			}
+			continue
+		}
+		if err != nil {
+			return fmt.Errorf("%w: failed to populate blob data cache: %w", errCacheWarmFailed, err)
+		}
+		if err := cache.ensure(ident); err != nil {
+			return fmt.Errorf("%w: failed to write cache entry for %s: %w", errCacheWarmFailed, l.sszPath(ident), err)
+		}
+	}
+	return nil
+}
+
+func migrateLayout(fs afero.Fs, from, to fsLayout, cache *blobStorageSummaryCache) error {
+	start := time.Now()
+	iter, err := from.iterateIdents(0)
+	if err != nil {
+		return errors.Wrapf(errMigrationFailure, "failed to iterate legacy structure while migrating blobs, err=%s", err.Error())
+	}
+	if iter.atEOF() {
+		return errLayoutNotDetected
+	}
+	log.WithField("fromLayout", from.name()).WithField("toLayout", to.name()).Info("Migrating blob filesystem layout. This one-time operation can take extra time (up to a few minutes for systems with extended blob storage and a cold disk cache).")
+	lastMoved := ""
+	parentDirs := make(map[string]bool) // this map should have < 65k keys by design
+	moved := 0
+	dc := newDirCleaner()
+	for ident, err := iter.next(); !errors.Is(err, io.EOF); ident, err = iter.next() {
+		if err != nil {
+			if errors.Is(err, errIdentFailure) {
+				idf := &identificationError{}
+				if errors.As(err, &idf) {
+					log.WithFields(idf.LogFields()).WithError(err).Error("Failed to migrate blob path")
+				}
+				continue
+			}
+			return errors.Wrapf(errMigrationFailure, "failed to iterate previous layout structure while migrating blobs, err=%s", err.Error())
+		}
+		src := from.dir(ident)
+		target := to.dir(ident)
+		if src != lastMoved {
+			targetParent := filepath.Dir(target)
+			if targetParent != "" && targetParent != "." && !parentDirs[targetParent] {
+				if err := fs.MkdirAll(targetParent, directoryPermissions()); err != nil {
+					return errors.Wrapf(errMigrationFailure, "failed to make enclosing path before moving %s to %s", src, target)
+				}
+				parentDirs[targetParent] = true
+			}
+			if err := fs.Rename(src, target); err != nil {
+				return errors.Wrapf(errMigrationFailure, "could not rename %s to %s", src, target)
+			}
+			moved += 1
+			lastMoved = src
+			for _, dir := range from.blockParentDirs(ident) {
+				dc.add(dir)
+			}
+		}
+		if err := cache.ensure(ident); err != nil {
+			return errors.Wrapf(errMigrationFailure, "could not cache path %s, err=%s", to.sszPath(ident), err.Error())
+		}
+	}
+	dc.clean(fs)
+	if moved > 0 {
+		log.WithField("dirsMoved", moved).WithField("elapsed", time.Since(start)).
+			Info("Blob filesystem migration complete.")
+	}
+	return nil
+}
+
+type dirCleaner struct {
+	maxDepth int
+	layers   map[int]map[string]struct{}
+}
+
+func newDirCleaner() *dirCleaner {
+	return &dirCleaner{layers: make(map[int]map[string]struct{})}
+}
+
+func (d *dirCleaner) add(dir string) {
+	nLayers := len(strings.Split(dir, string(filepath.Separator)))
+	_, ok := d.layers[nLayers]
+	if !ok {
+		d.layers[nLayers] = make(map[string]struct{})
+	}
+	d.layers[nLayers][dir] = struct{}{}
+	if nLayers > d.maxDepth {
+		d.maxDepth = nLayers
+	}
+}
+
+func (d *dirCleaner) clean(fs afero.Fs) {
+	for i := d.maxDepth; i >= 0; i-- {
+		d.cleanLayer(fs, i)
+	}
+}
+
+func (d *dirCleaner) cleanLayer(fs afero.Fs, layer int) {
+	dirs, ok := d.layers[layer]
+	if !ok {
+		return
+	}
+	for dir := range dirs {
+		// Use Remove rather than RemoveAll to make sure we're only removing empty directories
+		if err := fs.Remove(dir); err != nil {
+			log.WithField("dir", dir).WithError(err).Error("Failed to remove blob directory, please remove it manually if desired.")
+			contents, err := listDir(fs, dir)
+			if err != nil {
+				log.WithField("dir", dir).WithError(err).Error("Could not list blob directory contents to find reason for removal failure.")
+				continue
+			}
+			for _, c := range contents {
+				log.WithField("file", c).WithField("dir", dir).Debug("Unexpected file blocking migrated blob directory cleanup.")
+			}
+		}
+	}
+}
+
+type pruneSummary struct {
+	blobsPruned    int
+	failedRemovals []string
+}
+
+func (s pruneSummary) LogFields() logrus.Fields {
+	return logrus.Fields{
+		"blobsPruned":    s.blobsPruned,
+		"failedRemovals": len(s.failedRemovals),
+	}
+}
+
+func pruneBefore(before primitives.Epoch, l fsLayout) (map[primitives.Epoch]*pruneSummary, error) {
+	sums := make(map[primitives.Epoch]*pruneSummary)
+	iter, err := l.iterateIdents(before)
+	if err != nil {
+		return nil, errors.Wrap(err, "failed to iterate blob paths for pruning")
+	}
+
+	// We will get an ident for each index, but want to prune all indexes for the given root together.
+	var lastIdent blobIdent
+	for ident, err := iter.next(); !errors.Is(err, io.EOF); ident, err = iter.next() {
+		if err != nil {
+			if errors.Is(err, errIdentFailure) {
+				idf := &identificationError{}
+				if errors.As(err, &idf) {
+					log.WithFields(idf.LogFields()).WithError(err).Error("Failed to prune blob path due to identification errors")
+				}
+				continue
+			}
+			log.WithError(err).Error("encountered unhandled error during pruning")
+			return nil, errors.Wrap(errPruneFailed, err.Error())
+		}
+		if ident.epoch >= before {
+			continue
+		}
+		if lastIdent.root != ident.root {
+			pruneOne(lastIdent, l, sums)
+			lastIdent = ident
+		}
+	}
+	// handle the final ident
+	pruneOne(lastIdent, l, sums)
+
+	return sums, nil
+}
+
+func pruneOne(ident blobIdent, l fsLayout, sums map[primitives.Epoch]*pruneSummary) {
+	// Skip pruning the n-1 ident if we're on the first real ident (lastIdent will be zero value).
+	if ident.root == params.BeaconConfig().ZeroHash {
+		return
+	}
+	_, ok := sums[ident.epoch]
+	if !ok {
+		sums[ident.epoch] = &pruneSummary{}
+	}
+	s := sums[ident.epoch]
+	removed, err := l.remove(ident)
+	if err != nil {
+		s.failedRemovals = append(s.failedRemovals, l.dir(ident))
+		log.WithField("root", fmt.Sprintf("%#x", ident.root)).Error("Failed to delete blob directory for root")
+	}
+	s.blobsPruned += removed
+}
--- a/beacon-chain/db/filesystem/layout_by_epoch.go
+++ b/beacon-chain/db/filesystem/layout_by_epoch.go
@@ -0,0 +1,212 @@
+package filesystem
+
+import (
+	"fmt"
+	"os"
+	"path"
+	"path/filepath"
+	"strconv"
+
+	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/config/params"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/spf13/afero"
+)
+
+const epochsPerDirectory = 4096
+
+type periodicEpochLayout struct {
+	fs     afero.Fs
+	cache  *blobStorageSummaryCache
+	pruner *blobPruner
+}
+
+var _ fsLayout = &periodicEpochLayout{}
+
+func newPeriodicEpochLayout(fs afero.Fs, cache *blobStorageSummaryCache, pruner *blobPruner) fsLayout {
+	l := &periodicEpochLayout{fs: fs, cache: cache, pruner: pruner}
+	return l
+}
+
+func (l *periodicEpochLayout) name() string {
+	return LayoutNameByEpoch
+}
+
+func (l *periodicEpochLayout) blockParentDirs(ident blobIdent) []string {
+	return []string{
+		periodicEpochBaseDir,
+		l.periodDir(ident.epoch),
+		l.epochDir(ident.epoch),
+	}
+}
+
+func (l *periodicEpochLayout) notify(ident blobIdent) error {
+	if err := l.cache.ensure(ident); err != nil {
+		return err
+	}
+	l.pruner.notify(ident.epoch, l)
+	return nil
+}
+
+// If before == 0, it won't be used as a filter and all idents will be returned.
+func (l *periodicEpochLayout) iterateIdents(before primitives.Epoch) (*identIterator, error) {
+	_, err := l.fs.Stat(periodicEpochBaseDir)
+	if err != nil {
+		if os.IsNotExist(err) {
+			return &identIterator{eof: true}, nil // The directory is non-existent, which is fine; stop iteration.
+		}
+		return nil, errors.Wrapf(err, "error reading path %s", periodicEpochBaseDir)
+	}
+	// iterate root, which should have directories named by "period"
+	entries, err := listDir(l.fs, periodicEpochBaseDir)
+	if err != nil {
+		return nil, errors.Wrapf(err, "failed to list %s", periodicEpochBaseDir)
+	}
+
+	return &identIterator{
+		fs:   l.fs,
+		path: periodicEpochBaseDir,
+		// Please see comments on the `layers` field in `identIterator`` if the role of the layers is unclear.
+		layers: []layoutLayer{
+			{populateIdent: populateNoop, filter: isBeforePeriod(before)},
+			{populateIdent: populateEpoch, filter: isBeforeEpoch(before)},
+			{populateIdent: populateRoot, filter: isRootDir},  // extract root from path
+			{populateIdent: populateIndex, filter: isSszFile}, // extract index from filename
+		},
+		entries: entries,
+	}, nil
+}
+
+func (l *periodicEpochLayout) ident(root [32]byte, idx uint64) (blobIdent, error) {
+	return l.cache.identForIdx(root, idx)
+}
+
+func (l *periodicEpochLayout) dirIdent(root [32]byte) (blobIdent, error) {
+	return l.cache.identForRoot(root)
+}
+
+func (l *periodicEpochLayout) summary(root [32]byte) BlobStorageSummary {
+	return l.cache.Summary(root)
+}
+
+func (l *periodicEpochLayout) dir(n blobIdent) string {
+	return filepath.Join(l.epochDir(n.epoch), rootToString(n.root))
+}
+
+func (l *periodicEpochLayout) epochDir(epoch primitives.Epoch) string {
+	return filepath.Join(l.periodDir(epoch), fmt.Sprintf("%d", epoch))
+}
+
+func (l *periodicEpochLayout) periodDir(epoch primitives.Epoch) string {
+	return filepath.Join(periodicEpochBaseDir, fmt.Sprintf("%d", periodForEpoch(epoch)))
+}
+
+func (l *periodicEpochLayout) sszPath(n blobIdent) string {
+	return filepath.Join(l.dir(n), n.sszFname())
+}
+
+func (l *periodicEpochLayout) partPath(n blobIdent, entropy string) string {
+	return path.Join(l.dir(n), n.partFname(entropy))
+}
+
+func (l *periodicEpochLayout) pruneBefore(before primitives.Epoch) (*pruneSummary, error) {
+	sums, err := pruneBefore(before, l)
+	if err != nil {
+		return nil, err
+	}
+	// Roll up summaries and clean up per-epoch directories.
+	rollup := &pruneSummary{}
+	for epoch, sum := range sums {
+		rollup.blobsPruned += sum.blobsPruned
+		rollup.failedRemovals = append(rollup.failedRemovals, sum.failedRemovals...)
+		rmdir := l.epochDir(epoch)
+		if len(sum.failedRemovals) == 0 {
+			if err := l.fs.Remove(rmdir); err != nil {
+				log.WithField("dir", rmdir).WithError(err).Error("Failed to remove epoch directory while pruning")
+			}
+		} else {
+			log.WithField("dir", rmdir).WithField("numFailed", len(sum.failedRemovals)).WithError(err).Error("Unable to remove epoch directory due to pruning failures")
+		}
+	}
+
+	return rollup, nil
+}
+
+func (l *periodicEpochLayout) remove(ident blobIdent) (int, error) {
+	removed := l.cache.evict(ident.root)
+	// Skip the syscall if there are no blobs to remove.
+	if removed == 0 {
+		return 0, nil
+	}
+	if err := l.fs.RemoveAll(l.dir(ident)); err != nil {
+		return removed, err
+	}
+	return removed, nil
+}
+
+func periodForEpoch(epoch primitives.Epoch) primitives.Epoch {
+	return epoch / params.BeaconConfig().MinEpochsForBlobsSidecarsRequest
+}
+
+// Funcs below this line are iteration support methods that are specific to the epoch layout.
+
+func isBeforePeriod(before primitives.Epoch) func(string) bool {
+	if before == 0 {
+		return filterNoop
+	}
+	beforePeriod := periodForEpoch(before)
+	if before%epochsPerDirectory != 0 {
+		// Add one because we need to include the period the epoch is in, unless it is the first epoch in the period,
+		// in which case we can just look at any previous period.
+		beforePeriod += 1
+	}
+	return func(p string) bool {
+		period, err := periodFromPath(p)
+		if err != nil {
+			return false
+		}
+		return primitives.Epoch(period) < beforePeriod
+	}
+}
+
+func isBeforeEpoch(before primitives.Epoch) func(string) bool {
+	if before == 0 {
+		return filterNoop
+	}
+	return func(p string) bool {
+		epoch, err := epochFromPath(p)
+		if err != nil {
+			return false
+		}
+		return epoch < before
+	}
+}
+
+func epochFromPath(p string) (primitives.Epoch, error) {
+	subdir := filepath.Base(p)
+	epoch, err := strconv.ParseUint(subdir, 10, 64)
+	if err != nil {
+		return 0, errors.Wrapf(errInvalidDirectoryLayout,
+			"failed to decode epoch as uint, err=%s, dir=%s", err.Error(), p)
+	}
+	return primitives.Epoch(epoch), nil
+}
+
+func periodFromPath(p string) (uint64, error) {
+	subdir := filepath.Base(p)
+	period, err := strconv.ParseUint(subdir, 10, 64)
+	if err != nil {
+		return 0, errors.Wrapf(errInvalidDirectoryLayout,
+			"failed to decode period from path as uint, err=%s, dir=%s", err.Error(), p)
+	}
+	return period, nil
+}
+
+func populateEpoch(namer blobIdent, dir string) (blobIdent, error) {
+	epoch, err := epochFromPath(dir)
+	if err != nil {
+		return namer, err
+	}
+	namer.epoch = epoch
+	return namer, nil
+}
--- a/beacon-chain/db/filesystem/layout_flat.go
+++ b/beacon-chain/db/filesystem/layout_flat.go
@@ -0,0 +1,219 @@
+package filesystem
+
+import (
+	"encoding/binary"
+	"io"
+	"os"
+	"path"
+
+	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
+	"github.com/spf13/afero"
+)
+
+type flatLayout struct {
+	fs     afero.Fs
+	cache  *blobStorageSummaryCache
+	pruner *blobPruner
+}
+
+var _ fsLayout = &flatLayout{}
+
+func newFlatLayout(fs afero.Fs, cache *blobStorageSummaryCache, pruner *blobPruner) fsLayout {
+	l := &flatLayout{fs: fs, cache: cache, pruner: pruner}
+	return l
+}
+
+func (l *flatLayout) iterateIdents(before primitives.Epoch) (*identIterator, error) {
+	if _, err := l.fs.Stat("."); err != nil {
+		if os.IsNotExist(err) {
+			return &identIterator{eof: true}, nil // The directory is non-existent, which is fine; stop iteration.
+		}
+		return nil, errors.Wrapf(err, "error reading path %s", periodicEpochBaseDir)
+	}
+	entries, err := listDir(l.fs, ".")
+	if err != nil {
+		return nil, errors.Wrapf(err, "could not list root directory")
+	}
+	slotAndIndex := &flatSlotReader{fs: l.fs, cache: l.cache, before: before}
+	return &identIterator{
+		fs: l.fs,
+		// Please see comments on the `layers` field in `identIterator`` if the role of the layers is unclear.
+		layers: []layoutLayer{
+			{populateIdent: populateRoot, filter: isFlatCachedAndBefore(l.cache, before)},
+			{populateIdent: slotAndIndex.populateEpoch, filter: slotAndIndex.isSSZAndBefore}},
+		entries: entries,
+	}, nil
+}
+
+func (*flatLayout) name() string {
+	return LayoutNameFlat
+}
+
+func (l *flatLayout) blockParentDirs(ident blobIdent) []string {
+	return []string{}
+}
+
+func (*flatLayout) dir(n blobIdent) string {
+	return rootToString(n.root)
+}
+
+func (l *flatLayout) sszPath(n blobIdent) string {
+	return path.Join(l.dir(n), n.sszFname())
+}
+
+func (l *flatLayout) partPath(n blobIdent, entropy string) string {
+	return path.Join(l.dir(n), n.partFname(entropy))
+}
+
+func (l *flatLayout) ident(root [32]byte, idx uint64) (blobIdent, error) {
+	return l.cache.identForIdx(root, idx)
+}
+
+func (l *flatLayout) dirIdent(root [32]byte) (blobIdent, error) {
+	return l.cache.identForRoot(root)
+}
+
+func (l *flatLayout) summary(root [32]byte) BlobStorageSummary {
+	return l.cache.Summary(root)
+}
+
+func (l *flatLayout) remove(ident blobIdent) (int, error) {
+	removed := l.cache.evict(ident.root)
+	if err := l.fs.RemoveAll(l.dir(ident)); err != nil {
+		return removed, err
+	}
+	return removed, nil
+}
+
+func (l *flatLayout) notify(ident blobIdent) error {
+	if err := l.cache.ensure(ident); err != nil {
+		return err
+	}
+	l.pruner.notify(ident.epoch, l)
+	return nil
+}
+
+func (l *flatLayout) pruneBefore(before primitives.Epoch) (*pruneSummary, error) {
+	sums, err := pruneBefore(before, l)
+	if err != nil {
+		return nil, err
+	}
+
+	// Roll up summaries and clean up per-epoch directories.
+	rollup := &pruneSummary{}
+	for _, sum := range sums {
+		rollup.blobsPruned += sum.blobsPruned
+		rollup.failedRemovals = append(rollup.failedRemovals, sum.failedRemovals...)
+	}
+
+	return rollup, nil
+}
+
+// Below this line are iteration support funcs and types that are specific to the flat layout.
+
+// Read slot from marshaled BlobSidecar data in the given file. See slotFromBlob for details.
+func slotFromFile(name string, fs afero.Fs) (primitives.Slot, error) {
+	f, err := fs.Open(name)
+	if err != nil {
+		return 0, err
+	}
+	defer func() {
+		if err := f.Close(); err != nil {
+			log.WithError(err).Errorf("Could not close blob file")
+		}
+	}()
+	return slotFromBlob(f)
+}
+
+// slotFromBlob reads the ssz data of a file at the specified offset (8 + 131072 + 48 + 48 = 131176 bytes),
+// which is calculated based on the size of the BlobSidecar struct and is based on the size of the fields
+// preceding the slot information within SignedBeaconBlockHeader.
+func slotFromBlob(at io.ReaderAt) (primitives.Slot, error) {
+	b := make([]byte, 8)
+	_, err := at.ReadAt(b, 131176)
+	if err != nil {
+		return 0, err
+	}
+	rawSlot := binary.LittleEndian.Uint64(b)
+	return primitives.Slot(rawSlot), nil
+}
+
+type flatSlotReader struct {
+	before primitives.Epoch
+	fs     afero.Fs
+	cache  *blobStorageSummaryCache
+}
+
+func (l *flatSlotReader) populateEpoch(ident blobIdent, fname string) (blobIdent, error) {
+	ident, err := populateIndex(ident, fname)
+	if err != nil {
+		return ident, err
+	}
+	sum, ok := l.cache.get(ident.root)
+	if ok {
+		ident.epoch = sum.epoch
+		// Return early if the index is already known to the cache.
+		if sum.HasIndex(ident.index) {
+			return ident, nil
+		}
+	} else {
+		// If the root is not in the cache, we need to read the slot from the file.
+		slot, err := slotFromFile(fname, l.fs)
+		if err != nil {
+			return ident, err
+		}
+		ident.epoch = slots.ToEpoch(slot)
+	}
+	return ident, l.cache.ensure(ident)
+}
+
+func (l *flatSlotReader) isSSZAndBefore(fname string) bool {
+	if !isSszFile(fname) {
+		return false
+	}
+	// If 'before' != 0, assuming isSSZAndBefore is used as a filter on the same layer with populateEpoch, this will typically
+	// call populateEpoch before the iteration code calls it. So we can guarantee that the cache gets populated
+	// in either case, because if it is filtered out here, we either have a malformed path (root can't be determined) in which case
+	// the filter code won't call it anyway, or we have a valid path and the cache will be populated before the epoch can be compared.
+	if l.before == 0 {
+		return true
+	}
+	ident, err := populateRoot(blobIdent{}, path.Dir(fname))
+	// Filter out the path if we can't determine its root.
+	if err != nil {
+		return false
+	}
+	ident, err = l.populateEpoch(ident, fname)
+	// Filter out the path if we can't determine its epoch or properly cache it.
+	if err != nil {
+		return false
+	}
+	return ident.epoch < l.before
+}
+
+// isFlatCachedAndBefore returns a filter callback function to exclude roots that are known to be after the given epoch
+// based on the cache. It's an opportunistic filter; if the cache is not populated, it will not attempt to populate it.
+// isSSZAndBefore on the other hand, is a strict filter that will only return true if the file is an SSZ file and
+// the epoch can be determined.
+func isFlatCachedAndBefore(cache *blobStorageSummaryCache, before primitives.Epoch) func(string) bool {
+	if before == 0 {
+		return isRootDir
+	}
+	return func(p string) bool {
+		if !isRootDir(p) {
+			return false
+		}
+		root, err := rootFromPath(p)
+		if err != nil {
+			return false
+		}
+		sum, ok := cache.get(root)
+		// If we don't know the epoch by looking at the root, don't try to filter it.
+		if !ok {
+			return true
+		}
+		return sum.epoch < before
+	}
+}
--- a/beacon-chain/db/filesystem/layout_test.go
+++ b/beacon-chain/db/filesystem/layout_test.go
@@ -0,0 +1,75 @@
+package filesystem
+
+import (
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+)
+
+type mockLayout struct {
+	pruneBeforeFunc func(primitives.Epoch) (*pruneSummary, error)
+}
+
+var _ fsLayout = &mockLayout{}
+
+func (m *mockLayout) name() string {
+	return "mock"
+}
+
+func (*mockLayout) dir(_ blobIdent) string {
+	return ""
+}
+
+func (*mockLayout) blockParentDirs(id blobIdent) []string {
+	return []string{}
+}
+
+func (*mockLayout) sszPath(_ blobIdent) string {
+	return ""
+}
+
+func (*mockLayout) partPath(_ blobIdent, _ string) string {
+	return ""
+}
+
+func (*mockLayout) iterateIdents(_ primitives.Epoch) (*identIterator, error) {
+	return nil, nil
+}
+
+func (*mockLayout) ident(_ [32]byte, _ uint64) (blobIdent, error) {
+	return blobIdent{}, nil
+}
+
+func (*mockLayout) dirIdent(_ [32]byte) (blobIdent, error) {
+	return blobIdent{}, nil
+}
+
+func (*mockLayout) summary(_ [32]byte) BlobStorageSummary {
+	return BlobStorageSummary{}
+}
+
+func (*mockLayout) notify(blobIdent) error {
+	return nil
+}
+
+func (m *mockLayout) pruneBefore(before primitives.Epoch) (*pruneSummary, error) {
+	return m.pruneBeforeFunc(before)
+}
+
+func (*mockLayout) remove(ident blobIdent) (int, error) {
+	return 0, nil
+}
+
+var _ fsLayout = &mockLayout{}
+
+func TestCleaner(t *testing.T) {
+	l := &periodicEpochLayout{}
+	p := l.periodDir(11235813)
+	e := l.epochDir(11235813)
+	dc := newDirCleaner()
+	dc.add(p)
+	require.Equal(t, 2, dc.maxDepth)
+	dc.add(e)
+	require.Equal(t, 3, dc.maxDepth)
+}
--- a/beacon-chain/db/filesystem/migration_test.go
+++ b/beacon-chain/db/filesystem/migration_test.go
@@ -0,0 +1,180 @@
+package filesystem
+
+import (
+	"os"
+	"testing"
+
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
+	"github.com/spf13/afero"
+)
+
+func ezIdent(t *testing.T, rootStr string, epoch primitives.Epoch, index uint64) blobIdent {
+	r, err := stringToRoot(rootStr)
+	require.NoError(t, err)
+	return blobIdent{root: r, epoch: epoch, index: index}
+}
+
+func setupTestBlobFile(t *testing.T, ident blobIdent, offset primitives.Slot, fs afero.Fs, l fsLayout) {
+	slot, err := slots.EpochStart(ident.epoch)
+	require.NoError(t, err)
+	slot += offset
+	_, sc := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 1)
+	scb, err := sc[0].MarshalSSZ()
+	require.NoError(t, err)
+	dir := l.dir(ident)
+	require.NoError(t, fs.MkdirAll(dir, directoryPermissions()))
+	p := l.sszPath(ident)
+	require.NoError(t, afero.WriteFile(fs, p, scb, 0666))
+	_, err = fs.Stat(p)
+	require.NoError(t, err)
+}
+
+type migrationTestTarget struct {
+	ident      blobIdent
+	slotOffset primitives.Slot
+	migrated   bool
+	path       string
+}
+
+func testAssertFsMigrated(t *testing.T, fs afero.Fs, ident blobIdent, before, after fsLayout) {
+	// Assert the pre-migration path is gone.
+	_, err := fs.Stat(before.sszPath(ident))
+	require.ErrorIs(t, err, os.ErrNotExist)
+	dir := before.dir(ident)
+	_, err = listDir(fs, dir)
+	require.ErrorIs(t, err, os.ErrNotExist)
+
+	// Assert the post-migration path present.
+	_, err = fs.Stat(after.sszPath(ident))
+	require.NoError(t, err)
+}
+
+func TestMigrations(t *testing.T) {
+	cases := []struct {
+		name           string
+		forwardLayout  string
+		backwardLayout string
+		targets        []migrationTestTarget
+	}{
+		{
+			name:           "all need migration",
+			backwardLayout: LayoutNameFlat,
+			forwardLayout:  LayoutNameByEpoch,
+			targets: []migrationTestTarget{
+				{
+					ident: ezIdent(t, "0x0125e54c64c925018c9296965a5b622d9f5ab626c10917860dcfb6aa09a0a00b", 1234, 0),
+				},
+				{
+					ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 0),
+					slotOffset: 31,
+				},
+				{
+					ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 1),
+					slotOffset: 31,
+				},
+				{
+					ident:      ezIdent(t, "0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c", 16777216, 0),
+					slotOffset: 16,
+				},
+			},
+		},
+		{
+			name:           "mix old and new",
+			backwardLayout: LayoutNameFlat,
+			forwardLayout:  LayoutNameByEpoch,
+			targets: []migrationTestTarget{
+				{
+					ident: ezIdent(t, "0x0125e54c64c925018c9296965a5b622d9f5ab626c10917860dcfb6aa09a0a00b", 1234, 0),
+				},
+				{
+					ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 0),
+					slotOffset: 31,
+				},
+				{
+					ident:      ezIdent(t, "0x0127dba6fd30fdbb47e73e861d5c6e602b38ac3ddc945bb6a2fc4e10761e9a86", 5330, 1),
+					slotOffset: 31,
+				},
+				{
+					ident:      ezIdent(t, "0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c", 16777216, 0),
+					slotOffset: 16,
+					migrated:   true,
+				},
+				{
+					ident:      ezIdent(t, "0x0232521756a0b965eab2c2245d7ad85feaeaf5f427cd14d1a7531f9d555b415c", 16777216, 1),
+					slotOffset: 16,
+					migrated:   true,
+				},
+				{
+					ident:      ezIdent(t, "0x42eabe3d2c125410cd226de6f2825fb7575ab896c3f52e43de1fa29e4c809aba", 16777217, 0),
+					slotOffset: 16,
+					migrated:   true,
+				},
+				{
+					ident:    ezIdent(t, "0x666cea5034e22bd3b849cb33914cad59afd88ee08e4d5bc0e997411c945fbc1d", 11235, 1),
+					migrated: true,
+				},
+			},
+		},
+	}
+
+	for _, c := range cases {
+		t.Run(c.name, func(t *testing.T) {
+			t.Run("forward", func(t *testing.T) {
+				testMigration(t, c.forwardLayout, c.backwardLayout, c.targets)
+			})
+			// run the same test in reverse - to cover both directions while making the test table smaller.
+			t.Run("backward", func(t *testing.T) {
+				testMigration(t, c.forwardLayout, c.backwardLayout, c.targets)
+			})
+		})
+	}
+}
+
+func testMigration(t *testing.T, forwardName, backwardName string, targets []migrationTestTarget) {
+	fs := afero.NewMemMapFs()
+	cache := newBlobStorageCache()
+	forward, err := newLayout(forwardName, fs, cache, nil)
+	require.NoError(t, err)
+	backward, err := newLayout(backwardName, fs, cache, nil)
+	require.NoError(t, err)
+	for _, tar := range targets {
+		if tar.migrated {
+			setupTestBlobFile(t, tar.ident, tar.slotOffset, fs, forward)
+		} else {
+			setupTestBlobFile(t, tar.ident, tar.slotOffset, fs, backward)
+		}
+	}
+	require.NoError(t, migrateLayout(fs, backward, forward, cache))
+	for _, tar := range targets {
+		// Make sure the file wound up in the right spot, according to the forward layout
+		// and that the old file is gone, according to the backward layout.
+		testAssertFsMigrated(t, fs, tar.ident, backward, forward)
+		entry, ok := cache.get(tar.ident.root)
+		// we only expect cache to be populated here by files that needed to be moved.
+		if !tar.migrated {
+			require.Equal(t, true, ok)
+			require.Equal(t, true, entry.HasIndex(tar.ident.index))
+			require.Equal(t, tar.ident.epoch, entry.epoch)
+		}
+	}
+
+	// Run migration in reverse - testing "undo"
+	cache = newBlobStorageCache()
+	forward, err = newLayout(forwardName, fs, cache, nil)
+	require.NoError(t, err)
+	backward, err = newLayout(backwardName, fs, cache, nil)
+	require.NoError(t, err)
+	// forward and backward are flipped compared to the above
+	require.NoError(t, migrateLayout(fs, forward, backward, cache))
+	for _, tar := range targets {
+		// just like the above, but forward and backward are flipped
+		testAssertFsMigrated(t, fs, tar.ident, forward, backward)
+		entry, ok := cache.get(tar.ident.root)
+		require.Equal(t, true, ok)
+		require.Equal(t, true, entry.HasIndex(tar.ident.index))
+		require.Equal(t, tar.ident.epoch, entry.epoch)
+	}
+}
--- a/beacon-chain/db/filesystem/mock.go
+++ b/beacon-chain/db/filesystem/mock.go
@@ -4,30 +4,41 @@ import (
 	"testing"

 	"github.com/prysmaticlabs/prysm/v5/config/params"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
 	"github.com/spf13/afero"
 )

 // NewEphemeralBlobStorage should only be used for tests.
 // The instance of BlobStorage returned is backed by an in-memory virtual filesystem,
 // improving test performance and simplifying cleanup.
-func NewEphemeralBlobStorage(t testing.TB) *BlobStorage {
-	fs := afero.NewMemMapFs()
-	pruner, err := newBlobPruner(fs, params.BeaconConfig().MinEpochsForBlobsSidecarsRequest, withWarmedCache())
-	if err != nil {
-		t.Fatal("test setup issue", err)
-	}
-	return &BlobStorage{fs: fs, pruner: pruner}
+func NewEphemeralBlobStorage(t testing.TB, opts ...BlobStorageOption) *BlobStorage {
+	return NewWarmedEphemeralBlobStorageUsingFs(t, afero.NewMemMapFs(), opts...)
 }

-// NewEphemeralBlobStorageWithFs can be used by tests that want access to the virtual filesystem
+// NewEphemeralBlobStorageAndFs can be used by tests that want access to the virtual filesystem
 // in order to interact with it outside the parameters of the BlobStorage api.
-func NewEphemeralBlobStorageWithFs(t testing.TB) (afero.Fs, *BlobStorage) {
+func NewEphemeralBlobStorageAndFs(t testing.TB, opts ...BlobStorageOption) (afero.Fs, *BlobStorage) {
 	fs := afero.NewMemMapFs()
-	pruner, err := newBlobPruner(fs, params.BeaconConfig().MinEpochsForBlobsSidecarsRequest, withWarmedCache())
+	bs := NewWarmedEphemeralBlobStorageUsingFs(t, fs, opts...)
+	return fs, bs
+}
+
+func NewEphemeralBlobStorageUsingFs(t testing.TB, fs afero.Fs, opts ...BlobStorageOption) *BlobStorage {
+	opts = append(opts,
+		WithBlobRetentionEpochs(params.BeaconConfig().MinEpochsForBlobsSidecarsRequest),
+		WithFs(fs))
+	bs, err := NewBlobStorage(opts...)
 	if err != nil {
-		t.Fatal("test setup issue", err)
+		t.Fatalf("error initializing test BlobStorage, err=%s", err.Error())
 	}
-	return fs, &BlobStorage{fs: fs, pruner: pruner}
+	return bs
+}
+
+func NewWarmedEphemeralBlobStorageUsingFs(t testing.TB, fs afero.Fs, opts ...BlobStorageOption) *BlobStorage {
+	bs := NewEphemeralBlobStorageUsingFs(t, fs, opts...)
+	bs.WarmCache()
+	return bs
 }

 type BlobMocker struct {
@@ -37,17 +48,9 @@ type BlobMocker struct {

 // CreateFakeIndices creates empty blob sidecar files at the expected path for the given
 // root and indices to influence the result of Indices().
-func (bm *BlobMocker) CreateFakeIndices(root [32]byte, indices ...uint64) error {
+func (bm *BlobMocker) CreateFakeIndices(root [32]byte, slot primitives.Slot, indices ...uint64) error {
 	for i := range indices {
-		n := blobNamer{root: root, index: indices[i]}
-		if err := bm.fs.MkdirAll(n.dir(), directoryPermissions); err != nil {
-			return err
-		}
-		f, err := bm.fs.Create(n.path())
-		if err != nil {
-			return err
-		}
-		if err := f.Close(); err != nil {
+		if err := bm.bs.layout.notify(newBlobIdent(root, slots.ToEpoch(slot), indices[i])); err != nil {
 			return err
 		}
 	}
@@ -56,9 +59,8 @@ func (bm *BlobMocker) CreateFakeIndices(root [32]byte, indices ...uint64) error

 // NewEphemeralBlobStorageWithMocker returns a *BlobMocker value in addition to the BlobStorage value.
 // BlockMocker encapsulates things blob path construction to avoid leaking implementation details.
-func NewEphemeralBlobStorageWithMocker(_ testing.TB) (*BlobMocker, *BlobStorage) {
-	fs := afero.NewMemMapFs()
-	bs := &BlobStorage{fs: fs}
+func NewEphemeralBlobStorageWithMocker(t testing.TB) (*BlobMocker, *BlobStorage) {
+	fs, bs := NewEphemeralBlobStorageAndFs(t)
 	return &BlobMocker{fs: fs, bs: bs}, bs
 }

@@ -66,7 +68,7 @@ func NewMockBlobStorageSummarizer(t *testing.T, set map[[32]byte][]int) BlobStor
 	c := newBlobStorageCache()
 	for k, v := range set {
 		for i := range v {
-			if err := c.ensure(k, 0, uint64(v[i])); err != nil {
+			if err := c.ensure(blobIdent{root: k, epoch: 0, index: uint64(v[i])}); err != nil {
 				t.Fatal(err)
 			}
 		}
--- a/beacon-chain/db/filesystem/pruner.go
+++ b/beacon-chain/db/filesystem/pruner.go
@@ -1,319 +1,67 @@
 package filesystem

 import (
-	"context"
-	"encoding/binary"
-	"io"
-	"path"
-	"path/filepath"
-	"strconv"
-	"strings"
 	"sync"
 	"sync/atomic"
 	"time"

 	"github.com/pkg/errors"
-	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
-	"github.com/prysmaticlabs/prysm/v5/time/slots"
 	"github.com/sirupsen/logrus"
-	"github.com/spf13/afero"
 )

 const retentionBuffer primitives.Epoch = 2

-var (
-	errPruningFailures = errors.New("blobs could not be pruned for some roots")
-	errNotBlobSSZ      = errors.New("not a blob ssz file")
-)
+var errNotBlobSSZ = errors.New("not a blob ssz file")

+// blobPruner keeps track of the tail end of the retention period, based only the blobs it has seen via the notify method.
+// If the retention period advances in response to notify being called,
+// the pruner will invoke the pruneBefore method of the given layout in a new goroutine.
+// The details of pruning are left entirely to the layout, with the pruner's only responsibility being to
+// schedule just one pruning operation at a time, for each forward movement of the minimum retention epoch.
 type blobPruner struct {
-	sync.Mutex
-	prunedBefore atomic.Uint64
-	windowSize   primitives.Slot
-	cache        *blobStorageCache
-	cacheReady   chan struct{}
-	warmed       bool
-	fs           afero.Fs
+	mu              sync.Mutex
+	prunedBefore    atomic.Uint64
+	retentionPeriod primitives.Epoch
 }

-type prunerOpt func(*blobPruner) error
-
-func withWarmedCache() prunerOpt {
-	return func(p *blobPruner) error {
-		return p.warmCache()
-	}
+func newBlobPruner(retain primitives.Epoch) *blobPruner {
+	p := &blobPruner{retentionPeriod: retain + retentionBuffer}
+	return p
 }

-func newBlobPruner(fs afero.Fs, retain primitives.Epoch, opts ...prunerOpt) (*blobPruner, error) {
-	r, err := slots.EpochStart(retain + retentionBuffer)
-	if err != nil {
-		return nil, errors.Wrap(err, "could not set retentionSlots")
-	}
-	cw := make(chan struct{})
-	p := &blobPruner{fs: fs, windowSize: r, cache: newBlobStorageCache(), cacheReady: cw}
-	for _, o := range opts {
-		if err := o(p); err != nil {
-			return nil, err
-		}
-	}
-	return p, nil
-}
-
-// notify updates the pruner's view of root->blob mappings. This allows the pruner to build a cache
-// of root->slot mappings and decide when to evict old blobs based on the age of present blobs.
-func (p *blobPruner) notify(root [32]byte, latest primitives.Slot, idx uint64) error {
-	if err := p.cache.ensure(root, latest, idx); err != nil {
-		return err
-	}
-	pruned := uint64(windowMin(latest, p.windowSize))
-	if p.prunedBefore.Swap(pruned) == pruned {
-		return nil
+// notify returns a channel that is closed when the pruning operation is complete.
+// This is useful for tests, but at runtime fsLayouts or BlobStorage should not wait for completion.
+func (p *blobPruner) notify(latest primitives.Epoch, layout fsLayout) chan struct{} {
+	done := make(chan struct{})
+	floor := periodFloor(latest, p.retentionPeriod)
+	if primitives.Epoch(p.prunedBefore.Swap(uint64(floor))) >= floor {
+		// Only trigger pruning if the atomic swap changed the previous value of prunedBefore.
+		close(done)
+		return done
 	}
 	go func() {
-		p.Lock()
-		defer p.Unlock()
-		if err := p.prune(primitives.Slot(pruned)); err != nil {
-			log.WithError(err).Errorf("Failed to prune blobs from slot %d", latest)
+		p.mu.Lock()
+		start := time.Now()
+		defer p.mu.Unlock()
+		sum, err := layout.pruneBefore(floor)
+		if err != nil {
+			log.WithError(err).WithFields(sum.LogFields()).Warn("Encountered errors during blob pruning.")
 		}
+		log.WithFields(logrus.Fields{
+			"upToEpoch":    floor,
+			"duration":     time.Since(start).String(),
+			"filesRemoved": sum.blobsPruned,
+		}).Debug("Pruned old blobs")
+		blobsPrunedCounter.Add(float64(sum.blobsPruned))
+		close(done)
 	}()
-	return nil
+	return done
 }

-func windowMin(latest, offset primitives.Slot) primitives.Slot {
-	// Safely compute the first slot in the epoch for the latest slot
-	latest = latest - latest%params.BeaconConfig().SlotsPerEpoch
-	if latest < offset {
+func periodFloor(latest, period primitives.Epoch) primitives.Epoch {
+	if latest < period {
 		return 0
 	}
-	return latest - offset
-}
-
-func (p *blobPruner) warmCache() error {
-	p.Lock()
-	defer func() {
-		if !p.warmed {
-			p.warmed = true
-			close(p.cacheReady)
-		}
-		p.Unlock()
-	}()
-	if err := p.prune(0); err != nil {
-		return err
-	}
-	return nil
-}
-
-func (p *blobPruner) waitForCache(ctx context.Context) (*blobStorageCache, error) {
-	select {
-	case <-p.cacheReady:
-		return p.cache, nil
-	case <-ctx.Done():
-		return nil, ctx.Err()
-	}
-}
-
-// Prune prunes blobs in the base directory based on the retention epoch.
-// It deletes blobs older than currentEpoch - (retentionEpochs+bufferEpochs).
-// This is so that we keep a slight buffer and blobs are deleted after n+2 epochs.
-func (p *blobPruner) prune(pruneBefore primitives.Slot) error {
-	start := time.Now()
-	totalPruned, totalErr := 0, 0
-	// Customize logging/metrics behavior for the initial cache warmup when slot=0.
-	// We'll never see a prune request for slot 0, unless this is the initial call to warm up the cache.
-	if pruneBefore == 0 {
-		defer func() {
-			log.WithField("duration", time.Since(start).String()).Debug("Warmed up pruner cache")
-		}()
-	} else {
-		defer func() {
-			log.WithFields(logrus.Fields{
-				"upToEpoch":    slots.ToEpoch(pruneBefore),
-				"duration":     time.Since(start).String(),
-				"filesRemoved": totalPruned,
-			}).Debug("Pruned old blobs")
-			blobsPrunedCounter.Add(float64(totalPruned))
-		}()
-	}
-
-	entries, err := listDir(p.fs, ".")
-	if err != nil {
-		return errors.Wrap(err, "unable to list root blobs directory")
-	}
-	dirs := filter(entries, filterRoot)
-	for _, dir := range dirs {
-		pruned, err := p.tryPruneDir(dir, pruneBefore)
-		if err != nil {
-			totalErr += 1
-			log.WithError(err).WithField("directory", dir).Error("Unable to prune directory")
-		}
-		totalPruned += pruned
-	}
-
-	if totalErr > 0 {
-		return errors.Wrapf(errPruningFailures, "pruning failed for %d root directories", totalErr)
-	}
-	return nil
-}
-
-func shouldRetain(slot, pruneBefore primitives.Slot) bool {
-	return slot >= pruneBefore
-}
-
-func (p *blobPruner) tryPruneDir(dir string, pruneBefore primitives.Slot) (int, error) {
-	root, err := rootFromDir(dir)
-	if err != nil {
-		return 0, errors.Wrapf(err, "invalid directory, could not parse subdir as root %s", dir)
-	}
-	slot, slotCached := p.cache.slot(root)
-	// Return early if the slot is cached and doesn't need pruning.
-	if slotCached && shouldRetain(slot, pruneBefore) {
-		return 0, nil
-	}
-
-	// entries will include things that aren't ssz files, like dangling .part files. We need these to
-	// completely clean up the directory.
-	entries, err := listDir(p.fs, dir)
-	if err != nil {
-		return 0, errors.Wrapf(err, "failed to list blobs in directory %s", dir)
-	}
-	// scFiles filters the dir listing down to the ssz encoded BlobSidecar files. This allows us to peek
-	// at the first one in the list to figure out the slot.
-	scFiles := filter(entries, filterSsz)
-	if len(scFiles) == 0 {
-		log.WithField("dir", dir).Warn("Pruner ignoring directory with no blob files")
-		return 0, nil
-	}
-	if !slotCached {
-		slot, err = slotFromFile(path.Join(dir, scFiles[0]), p.fs)
-		if err != nil {
-			return 0, errors.Wrapf(err, "slot could not be read from blob file %s", scFiles[0])
-		}
-		for i := range scFiles {
-			idx, err := idxFromPath(scFiles[i])
-			if err != nil {
-				return 0, errors.Wrapf(err, "index could not be determined for blob file %s", scFiles[i])
-			}
-			if err := p.cache.ensure(root, slot, idx); err != nil {
-				return 0, errors.Wrapf(err, "could not update prune cache for blob file %s", scFiles[i])
-			}
-		}
-		if shouldRetain(slot, pruneBefore) {
-			return 0, nil
-		}
-	}
-
-	removed := 0
-	for _, fname := range entries {
-		fullName := path.Join(dir, fname)
-		if err := p.fs.Remove(fullName); err != nil {
-			return removed, errors.Wrapf(err, "unable to remove %s", fullName)
-		}
-		// Don't count other files that happen to be in the dir, like dangling .part files.
-		if filterSsz(fname) {
-			removed += 1
-		}
-		// Log a warning whenever we clean up a .part file
-		if filterPart(fullName) {
-			log.WithField("file", fullName).Warn("Deleting abandoned blob .part file")
-		}
-	}
-	if err := p.fs.Remove(dir); err != nil {
-		return removed, errors.Wrapf(err, "unable to remove blob directory %s", dir)
-	}
-
-	p.cache.evict(root)
-	return len(scFiles), nil
-}
-
-func idxFromPath(fname string) (uint64, error) {
-	fname = path.Base(fname)
-
-	if filepath.Ext(fname) != dotSszExt {
-		return 0, errors.Wrap(errNotBlobSSZ, "does not have .ssz extension")
-	}
-	parts := strings.Split(fname, ".")
-	if len(parts) != 2 {
-		return 0, errors.Wrap(errNotBlobSSZ, "unexpected filename structure (want <index>.ssz)")
-	}
-	return strconv.ParseUint(parts[0], 10, 64)
-}
-
-func rootFromDir(dir string) ([32]byte, error) {
-	subdir := filepath.Base(dir) // end of the path should be the blob directory, named by hex encoding of root
-	root, err := stringToRoot(subdir)
-	if err != nil {
-		return root, errors.Wrapf(err, "invalid directory, could not parse subdir as root %s", dir)
-	}
-	return root, nil
-}
-
-// Read slot from marshaled BlobSidecar data in the given file. See slotFromBlob for details.
-func slotFromFile(file string, fs afero.Fs) (primitives.Slot, error) {
-	f, err := fs.Open(file)
-	if err != nil {
-		return 0, err
-	}
-	defer func() {
-		if err := f.Close(); err != nil {
-			log.WithError(err).Errorf("Could not close blob file")
-		}
-	}()
-	return slotFromBlob(f)
-}
-
-// slotFromBlob reads the ssz data of a file at the specified offset (8 + 131072 + 48 + 48 = 131176 bytes),
-// which is calculated based on the size of the BlobSidecar struct and is based on the size of the fields
-// preceding the slot information within SignedBeaconBlockHeader.
-func slotFromBlob(at io.ReaderAt) (primitives.Slot, error) {
-	b := make([]byte, 8)
-	_, err := at.ReadAt(b, 131176)
-	if err != nil {
-		return 0, err
-	}
-	rawSlot := binary.LittleEndian.Uint64(b)
-	return primitives.Slot(rawSlot), nil
-}
-
-func listDir(fs afero.Fs, dir string) ([]string, error) {
-	top, err := fs.Open(dir)
-	if err != nil {
-		return nil, errors.Wrap(err, "failed to open directory descriptor")
-	}
-	defer func() {
-		if err := top.Close(); err != nil {
-			log.WithError(err).Errorf("Could not close file %s", dir)
-		}
-	}()
-	// re the -1 param: "If n <= 0, Readdirnames returns all the names from the directory in a single slice"
-	dirs, err := top.Readdirnames(-1)
-	if err != nil {
-		return nil, errors.Wrap(err, "failed to read directory listing")
-	}
-	return dirs, nil
-}
-
-func filter(entries []string, filt func(string) bool) []string {
-	filtered := make([]string, 0, len(entries))
-	for i := range entries {
-		if filt(entries[i]) {
-			filtered = append(filtered, entries[i])
-		}
-	}
-	return filtered
-}
-
-func filterRoot(s string) bool {
-	return strings.HasPrefix(s, "0x")
-}
-
-var dotSszExt = "." + sszExt
-var dotPartExt = "." + partExt
-
-func filterSsz(s string) bool {
-	return filepath.Ext(s) == dotSszExt
-}
-
-func filterPart(s string) bool {
-	return filepath.Ext(s) == dotPartExt
+	return latest - period
 }
--- a/beacon-chain/db/filesystem/pruner_test.go
+++ b/beacon-chain/db/filesystem/pruner_test.go
@@ -1,394 +1,197 @@
 package filesystem

 import (
-	"bytes"
-	"context"
-	"fmt"
-	"math"
+	"encoding/binary"
 	"os"
-	"path"
-	"sort"
 	"testing"
-	"time"

 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/verification"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
-	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
 	"github.com/spf13/afero"
 )

-func TestTryPruneDir_CachedNotExpired(t *testing.T) {
-	fs := afero.NewMemMapFs()
-	pr, err := newBlobPruner(fs, 0)
-	require.NoError(t, err)
-	slot := pr.windowSize
-	_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, params.BeaconConfig().MaxBlobsPerBlock(slot))
-	sc, err := verification.BlobSidecarNoop(sidecars[0])
-	require.NoError(t, err)
-	rootStr := rootString(sc.BlockRoot())
-	// This slot is right on the edge of what would need to be pruned, so by adding it to the cache and
-	// skipping any other test setup, we can be certain the hot cache path never touches the filesystem.
-	require.NoError(t, pr.cache.ensure(sc.BlockRoot(), sc.Slot(), 0))
-	pruned, err := pr.tryPruneDir(rootStr, pr.windowSize)
-	require.NoError(t, err)
-	require.Equal(t, 0, pruned)
+type prunerScenario struct {
+	name            string
+	prunedBefore    primitives.Epoch
+	retentionPeriod primitives.Epoch
+	latest          primitives.Epoch
+	expected        pruneExpectation
 }

-func TestCacheWarmFail(t *testing.T) {
-	fs := afero.NewMemMapFs()
-	n := blobNamer{root: bytesutil.ToBytes32([]byte("derp")), index: 0}
-	bp := n.path()
-	mkdir := path.Dir(bp)
-	require.NoError(t, fs.MkdirAll(mkdir, directoryPermissions))
-
-	// Create an empty blob index in the fs by touching the file at a seemingly valid path.
-	fi, err := fs.Create(bp)
-	require.NoError(t, err)
-	require.NoError(t, fi.Close())
-
-	// Cache warm should fail due to the unexpected EOF.
-	pr, err := newBlobPruner(fs, 0)
-	require.NoError(t, err)
-	require.ErrorIs(t, pr.warmCache(), errPruningFailures)
-
-	// The cache warm has finished, so calling waitForCache with a super short deadline
-	// should not block or hit the context deadline.
-	ctx := context.Background()
-	ctx, cancel := context.WithDeadline(ctx, time.Now().Add(1*time.Millisecond))
-	defer cancel()
-	c, err := pr.waitForCache(ctx)
-	// We will get an error and a nil value for the cache if we hit the deadline.
-	require.NoError(t, err)
-	require.NotNil(t, c)
+type pruneExpectation struct {
+	called  bool
+	arg     primitives.Epoch
+	summary *pruneSummary
+	err     error
 }

-func TestTryPruneDir_CachedExpired(t *testing.T) {
-	t.Run("empty directory", func(t *testing.T) {
-		fs := afero.NewMemMapFs()
-		pr, err := newBlobPruner(fs, 0)
-		require.NoError(t, err)
-		var slot primitives.Slot = 0
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 1)
-		sc, err := verification.BlobSidecarNoop(sidecars[0])
-		require.NoError(t, err)
-		rootStr := rootString(sc.BlockRoot())
-		require.NoError(t, fs.Mkdir(rootStr, directoryPermissions)) // make empty directory
-		require.NoError(t, pr.cache.ensure(sc.BlockRoot(), sc.Slot(), 0))
-		pruned, err := pr.tryPruneDir(rootStr, slot+1)
-		require.NoError(t, err)
-		require.Equal(t, 0, pruned)
-	})
-	t.Run("blobs to delete", func(t *testing.T) {
-		fs, bs := NewEphemeralBlobStorageWithFs(t)
-		var slot primitives.Slot = 0
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 2)
-		scs, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-
-		require.NoError(t, bs.Save(scs[0]))
-		require.NoError(t, bs.Save(scs[1]))
-
-		// check that the root->slot is cached
-		root := scs[0].BlockRoot()
-		rootStr := rootString(root)
-		cs, cok := bs.pruner.cache.slot(scs[0].BlockRoot())
-		require.Equal(t, true, cok)
-		require.Equal(t, slot, cs)
-
-		// ensure that we see the saved files in the filesystem
-		files, err := listDir(fs, rootStr)
-		require.NoError(t, err)
-		require.Equal(t, 2, len(files))
-
-		pruned, err := bs.pruner.tryPruneDir(rootStr, slot+1)
-		require.NoError(t, err)
-		require.Equal(t, 2, pruned)
-		files, err = listDir(fs, rootStr)
-		require.ErrorIs(t, err, os.ErrNotExist)
-		require.Equal(t, 0, len(files))
-	})
+func (e *pruneExpectation) record(before primitives.Epoch) (*pruneSummary, error) {
+	e.called = true
+	e.arg = before
+	if e.summary == nil {
+		e.summary = &pruneSummary{}
+	}
+	return e.summary, e.err
 }

-func TestTryPruneDir_SlotFromFile(t *testing.T) {
-	t.Run("expired blobs deleted", func(t *testing.T) {
-		fs, bs := NewEphemeralBlobStorageWithFs(t)
-		var slot primitives.Slot = 0
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 2)
-		scs, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-
-		require.NoError(t, bs.Save(scs[0]))
-		require.NoError(t, bs.Save(scs[1]))
-
-		// check that the root->slot is cached
-		root := scs[0].BlockRoot()
-		rootStr := rootString(root)
-		cs, ok := bs.pruner.cache.slot(root)
-		require.Equal(t, true, ok)
-		require.Equal(t, slot, cs)
-		// evict it from the cache so that we trigger the file read path
-		bs.pruner.cache.evict(root)
-		_, ok = bs.pruner.cache.slot(root)
-		require.Equal(t, false, ok)
-
-		// ensure that we see the saved files in the filesystem
-		files, err := listDir(fs, rootStr)
-		require.NoError(t, err)
-		require.Equal(t, 2, len(files))
-
-		pruned, err := bs.pruner.tryPruneDir(rootStr, slot+1)
-		require.NoError(t, err)
-		require.Equal(t, 2, pruned)
-		files, err = listDir(fs, rootStr)
-		require.ErrorIs(t, err, os.ErrNotExist)
-		require.Equal(t, 0, len(files))
-	})
-	t.Run("not expired, intact", func(t *testing.T) {
-		fs, bs := NewEphemeralBlobStorageWithFs(t)
-		// Set slot equal to the window size, so it should be retained.
-		slot := bs.pruner.windowSize
-		_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 2)
-		scs, err := verification.BlobSidecarSliceNoop(sidecars)
-		require.NoError(t, err)
-
-		require.NoError(t, bs.Save(scs[0]))
-		require.NoError(t, bs.Save(scs[1]))
-
-		// Evict slot mapping from the cache so that we trigger the file read path.
-		root := scs[0].BlockRoot()
-		rootStr := rootString(root)
-		bs.pruner.cache.evict(root)
-		_, ok := bs.pruner.cache.slot(root)
-		require.Equal(t, false, ok)
-
-		// Ensure that we see the saved files in the filesystem.
-		files, err := listDir(fs, rootStr)
-		require.NoError(t, err)
-		require.Equal(t, 2, len(files))
-
-		// This should use the slotFromFile code (simulating restart).
-		// Setting pruneBefore == slot, so that the slot will be outside the window (at the boundary).
-		pruned, err := bs.pruner.tryPruneDir(rootStr, slot)
-		require.NoError(t, err)
-		require.Equal(t, 0, pruned)
-
-		// Ensure files are still present.
-		files, err = listDir(fs, rootStr)
-		require.NoError(t, err)
-		require.Equal(t, 2, len(files))
-	})
-}
-
-func TestSlotFromBlob(t *testing.T) {
-	cases := []struct {
-		slot primitives.Slot
-	}{
-		{slot: 0},
-		{slot: 2},
-		{slot: 1123581321},
-		{slot: math.MaxUint64},
+func TestPrunerNotify(t *testing.T) {
+	defaultRetention := params.BeaconConfig().MinEpochsForBlobsSidecarsRequest
+	cases := []prunerScenario{
+		{
+			name:            "last epoch of period",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    11235,
+			latest:          defaultRetention + 11235,
+			expected:        pruneExpectation{called: false},
+		},
+		{
+			name:            "within period",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    11235,
+			latest:          11235 + defaultRetention - 1,
+			expected:        pruneExpectation{called: false},
+		},
+		{
+			name:            "triggers",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    11235,
+			latest:          11235 + 1 + defaultRetention,
+			expected:        pruneExpectation{called: true, arg: 11235 + 1},
+		},
+		{
+			name:            "from zero - before first period",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    0,
+			latest:          defaultRetention - 1,
+			expected:        pruneExpectation{called: false},
+		},
+		{
+			name:            "from zero - at boundary",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    0,
+			latest:          defaultRetention,
+			expected:        pruneExpectation{called: false},
+		},
+		{
+			name:            "from zero - triggers",
+			retentionPeriod: defaultRetention,
+			prunedBefore:    0,
+			latest:          defaultRetention + 1,
+			expected:        pruneExpectation{called: true, arg: 1},
+		},
 	}
 	for _, c := range cases {
-		t.Run(fmt.Sprintf("slot %d", c.slot), func(t *testing.T) {
-			_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, c.slot, 1)
-			sc := sidecars[0]
-			enc, err := sc.MarshalSSZ()
-			require.NoError(t, err)
-			slot, err := slotFromBlob(bytes.NewReader(enc))
-			require.NoError(t, err)
-			require.Equal(t, c.slot, slot)
+		t.Run(c.name, func(t *testing.T) {
+			actual := &pruneExpectation{}
+			l := &mockLayout{pruneBeforeFunc: actual.record}
+			pruner := &blobPruner{retentionPeriod: c.retentionPeriod}
+			pruner.prunedBefore.Store(uint64(c.prunedBefore))
+			done := pruner.notify(c.latest, l)
+			<-done
+			require.Equal(t, c.expected.called, actual.called)
+			require.Equal(t, c.expected.arg, actual.arg)
 		})
 	}
 }

-func TestSlotFromFile(t *testing.T) {
-	cases := []struct {
-		slot primitives.Slot
-	}{
-		{slot: 0},
-		{slot: 2},
-		{slot: 1123581321},
-		{slot: math.MaxUint64},
-	}
-	for _, c := range cases {
-		t.Run(fmt.Sprintf("slot %d", c.slot), func(t *testing.T) {
-			fs, bs := NewEphemeralBlobStorageWithFs(t)
-			_, sidecars := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, c.slot, 1)
-			sc, err := verification.BlobSidecarNoop(sidecars[0])
-			require.NoError(t, err)
-			require.NoError(t, bs.Save(sc))
-			fname := namerForSidecar(sc)
-			sszPath := fname.path()
-			slot, err := slotFromFile(sszPath, fs)
-			require.NoError(t, err)
-			require.Equal(t, c.slot, slot)
-		})
-	}
-}
-
-type dirFiles struct {
-	name     string
-	isDir    bool
-	children []dirFiles
-}
-
-func (df dirFiles) reify(t *testing.T, fs afero.Fs, base string) {
-	fullPath := path.Join(base, df.name)
-	if df.isDir {
-		if df.name != "" {
-			require.NoError(t, fs.Mkdir(fullPath, directoryPermissions))
-		}
-		for _, c := range df.children {
-			c.reify(t, fs, fullPath)
-		}
-	} else {
-		fp, err := fs.Create(fullPath)
+func testSetupBlobIdentPaths(t *testing.T, fs afero.Fs, bs *BlobStorage, idents []testIdent) []blobIdent {
+	created := make([]blobIdent, len(idents))
+	for i, id := range idents {
+		slot, err := slots.EpochStart(id.epoch)
 		require.NoError(t, err)
-		_, err = fp.WriteString("derp")
+		slot += id.offset
+		_, scs := util.GenerateTestDenebBlockWithSidecar(t, [32]byte{}, slot, 1)
+		sc := verification.FakeVerifyForTest(t, scs[0])
+		require.NoError(t, bs.Save(sc))
+		ident := identForSidecar(sc)
+		_, err = fs.Stat(bs.layout.sszPath(ident))
+		require.NoError(t, err)
+		created[i] = ident
+	}
+	return created
+}
+
+func testAssertBlobsPruned(t *testing.T, fs afero.Fs, bs *BlobStorage, pruned, remain []blobIdent) {
+	for _, id := range pruned {
+		_, err := fs.Stat(bs.layout.sszPath(id))
+		require.NotNil(t, err)
+		require.Equal(t, true, os.IsNotExist(err))
+	}
+	for _, id := range remain {
+		_, err := fs.Stat(bs.layout.sszPath(id))
 		require.NoError(t, err)
 	}
 }

-func (df dirFiles) childNames() []string {
-	cn := make([]string, len(df.children))
-	for i := range df.children {
-		cn[i] = df.children[i].name
-	}
-	return cn
+type testIdent struct {
+	blobIdent
+	offset primitives.Slot
 }

-func TestListDir(t *testing.T) {
-	fs := afero.NewMemMapFs()
-
-	// parent directory
-	fsLayout := dirFiles{isDir: true}
-	// break out each subdir for easier assertions
-	notABlob := dirFiles{name: "notABlob", isDir: true}
-	childlessBlob := dirFiles{name: "0x0987654321", isDir: true}
-	blobWithSsz := dirFiles{name: "0x1123581321", isDir: true,
-		children: []dirFiles{{name: "1.ssz"}, {name: "2.ssz"}},
+func testRoots(n int) [][32]byte {
+	roots := make([][32]byte, n)
+	for i := range roots {
+		binary.LittleEndian.PutUint32(roots[i][:], uint32(1+i))
 	}
-	blobWithSszAndTmp := dirFiles{name: "0x1234567890", isDir: true,
-		children: []dirFiles{{name: "5.ssz"}, {name: "0.part"}}}
-	fsLayout.children = append(fsLayout.children,
-		notABlob, childlessBlob, blobWithSsz, blobWithSszAndTmp)
+	return roots
+}

-	topChildren := make([]string, len(fsLayout.children))
-	for i := range fsLayout.children {
-		topChildren[i] = fsLayout.children[i].name
-	}
-
-	fsLayout.reify(t, fs, "")
+func TestLayoutPruneBefore(t *testing.T) {
+	roots := testRoots(10)
 	cases := []struct {
-		name     string
-		dirPath  string
-		expected []string
-		filter   func(string) bool
-		err      error
+		name        string
+		pruned      []testIdent
+		remain      []testIdent
+		pruneBefore primitives.Epoch
+		err         error
+		sum         pruneSummary
 	}{
 		{
-			name:     "non-existent",
-			dirPath:  "derp",
-			expected: []string{},
-			err:      os.ErrNotExist,
-		},
-		{
-			name:     "empty",
-			dirPath:  childlessBlob.name,
-			expected: []string{},
-		},
-		{
-			name:     "top",
-			dirPath:  ".",
-			expected: topChildren,
-		},
-		{
-			name:     "custom filter: only notABlob",
-			dirPath:  ".",
-			expected: []string{notABlob.name},
-			filter: func(s string) bool {
-				return s == notABlob.name
+			name:        "none pruned",
+			pruneBefore: 1,
+			pruned:      []testIdent{},
+			remain: []testIdent{
+				{offset: 1, blobIdent: blobIdent{root: roots[0], epoch: 1, index: 0}},
+				{offset: 1, blobIdent: blobIdent{root: roots[1], epoch: 1, index: 0}},
 			},
 		},
 		{
-			name:     "root filter",
-			dirPath:  ".",
-			expected: []string{childlessBlob.name, blobWithSsz.name, blobWithSszAndTmp.name},
-			filter:   filterRoot,
-		},
-		{
-			name:     "ssz filter",
-			dirPath:  blobWithSsz.name,
-			expected: blobWithSsz.childNames(),
-			filter:   filterSsz,
-		},
-		{
-			name:     "ssz mixed filter",
-			dirPath:  blobWithSszAndTmp.name,
-			expected: []string{"5.ssz"},
-			filter:   filterSsz,
+			name:        "expected pruned before epoch",
+			pruneBefore: 3,
+			pruned: []testIdent{
+				{offset: 0, blobIdent: blobIdent{root: roots[0], epoch: 1, index: 0}},
+				{offset: 31, blobIdent: blobIdent{root: roots[1], epoch: 1, index: 5}},
+				{offset: 0, blobIdent: blobIdent{root: roots[2], epoch: 2, index: 0}},
+				{offset: 31, blobIdent: blobIdent{root: roots[3], epoch: 2, index: 3}},
+			},
+			remain: []testIdent{
+				{offset: 0, blobIdent: blobIdent{root: roots[4], epoch: 3, index: 2}},  // boundary
+				{offset: 31, blobIdent: blobIdent{root: roots[5], epoch: 3, index: 0}}, // boundary
+				{offset: 0, blobIdent: blobIdent{root: roots[6], epoch: 4, index: 1}},
+				{offset: 31, blobIdent: blobIdent{root: roots[7], epoch: 4, index: 5}},
+			},
+			sum: pruneSummary{blobsPruned: 4},
 		},
 	}
 	for _, c := range cases {
 		t.Run(c.name, func(t *testing.T) {
-			result, err := listDir(fs, c.dirPath)
-			if c.filter != nil {
-				result = filter(result, c.filter)
-			}
-			if c.err != nil {
-				require.ErrorIs(t, err, c.err)
-				require.Equal(t, 0, len(result))
-			} else {
-				require.NoError(t, err)
-				sort.Strings(c.expected)
-				sort.Strings(result)
-				require.DeepEqual(t, c.expected, result)
-			}
-		})
-	}
-}
-
-func TestRootFromDir(t *testing.T) {
-	cases := []struct {
-		name string
-		dir  string
-		err  error
-		root [32]byte
-	}{
-		{
-			name: "happy path",
-			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cb",
-			root: [32]byte{255, 255, 135, 94, 29, 152, 92, 92, 203, 33, 72, 148, 152, 63, 36, 40,
-				237, 178, 113, 240, 248, 123, 104, 186, 112, 16, 228, 169, 157, 243, 181, 203},
-		},
-		{
-			name: "too short",
-			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5c",
-			err:  errInvalidRootString,
-		},
-		{
-			name: "too log",
-			dir:  "0xffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cbb",
-			err:  errInvalidRootString,
-		},
-		{
-			name: "missing prefix",
-			dir:  "ffff875e1d985c5ccb214894983f2428edb271f0f87b68ba7010e4a99df3b5cb",
-			err:  errInvalidRootString,
-		},
-	}
-	for _, c := range cases {
-		t.Run(c.name, func(t *testing.T) {
-			root, err := stringToRoot(c.dir)
+			fs, bs := NewEphemeralBlobStorageAndFs(t, WithLayout(LayoutNameByEpoch))
+			pruned := testSetupBlobIdentPaths(t, fs, bs, c.pruned)
+			remain := testSetupBlobIdentPaths(t, fs, bs, c.remain)
+			sum, err := bs.layout.pruneBefore(c.pruneBefore)
 			if c.err != nil {
 				require.ErrorIs(t, err, c.err)
 				return
 			}
 			require.NoError(t, err)
-			require.Equal(t, c.root, root)
+			testAssertBlobsPruned(t, fs, bs, pruned, remain)
+			require.Equal(t, c.sum.blobsPruned, sum.blobsPruned)
+			require.Equal(t, len(c.pruned), sum.blobsPruned)
+			require.Equal(t, len(c.sum.failedRemovals), len(sum.failedRemovals))
 		})
 	}
 }
--- a/beacon-chain/db/iface/interface.go
+++ b/beacon-chain/db/iface/interface.go
@@ -101,6 +101,7 @@ type NoHeadAccessDatabase interface {
 	SaveLightClientBootstrap(ctx context.Context, blockRoot []byte, bootstrap interfaces.LightClientBootstrap) error

 	CleanUpDirtyStates(ctx context.Context, slotsPerArchivedPoint primitives.Slot) error
+	DeleteHistoricalDataBeforeSlot(ctx context.Context, slot primitives.Slot) error
 }

 // HeadAccessDatabase defines a struct with access to reading chain head data.
--- a/beacon-chain/db/kv/blocks.go
+++ b/beacon-chain/db/kv/blocks.go
@@ -227,10 +227,7 @@ func (s *Store) DeleteBlock(ctx context.Context, root [32]byte) error {
 			return ErrDeleteJustifiedAndFinalized
 		}

-		if err := tx.Bucket(blocksBucket).Delete(root[:]); err != nil {
-			return err
-		}
-		if err := tx.Bucket(blockParentRootIndicesBucket).Delete(root[:]); err != nil {
+		if err := s.deleteBlock(tx, root[:]); err != nil {
 			return err
 		}
 		s.blockCache.Del(string(root[:]))
@@ -238,6 +235,89 @@ func (s *Store) DeleteBlock(ctx context.Context, root [32]byte) error {
 	})
 }

+// DeleteHistoricalDataBeforeSlot deletes all blocks and states before the given slot.
+// This function deletes data from the following buckets:
+// - blocksBucket
+// - blockParentRootIndicesBucket
+// - finalizedBlockRootsIndexBucket
+// - stateBucket
+// - stateSummaryBucket
+// - blockRootValidatorHashesBucket
+// - blockSlotIndicesBucket
+// - stateSlotIndicesBucket
+func (s *Store) DeleteHistoricalDataBeforeSlot(ctx context.Context, cutoffSlot primitives.Slot) error {
+	ctx, span := trace.StartSpan(ctx, "BeaconDB.DeleteHistoricalDataBeforeSlot")
+	defer span.End()
+
+	// Collect slot/root pairs to perform deletions in a separate read only transaction.
+	var (
+		roots [][]byte
+		slts  []primitives.Slot
+	)
+	err := s.db.View(func(tx *bolt.Tx) error {
+		var err error
+		roots, slts, err = blockRootsBySlotRange(ctx, tx.Bucket(blockSlotIndicesBucket), primitives.Slot(0), cutoffSlot, nil, nil, nil)
+		if err != nil {
+			return errors.Wrap(err, "could not retrieve block roots")
+		}
+		return nil
+	})
+	if err != nil {
+		return errors.Wrap(err, "could not retrieve block roots and slots")
+	}
+
+	// Perform all deletions in a single transaction for atomicity
+	return s.db.Update(func(tx *bolt.Tx) error {
+		for _, root := range roots {
+			// Delete block
+			if err = s.deleteBlock(tx, root); err != nil {
+				return err
+			}
+
+			// Delete finalized block roots index
+			if err = tx.Bucket(finalizedBlockRootsIndexBucket).Delete(root); err != nil {
+				return errors.Wrap(err, "could not delete finalized block root index")
+			}
+
+			// Delete state
+			if err = tx.Bucket(stateBucket).Delete(root); err != nil {
+				return errors.Wrap(err, "could not delete state")
+			}
+
+			// Delete state summary
+			if err = tx.Bucket(stateSummaryBucket).Delete(root); err != nil {
+				return errors.Wrap(err, "could not delete state summary")
+			}
+
+			// Delete validator entries
+			if err = s.deleteValidatorHashes(tx, root); err != nil {
+				return errors.Wrap(err, "could not delete validators")
+			}
+		}
+
+		for _, slot := range slts {
+			// Delete slot indices
+			if err = tx.Bucket(blockSlotIndicesBucket).Delete(bytesutil.SlotToBytesBigEndian(slot)); err != nil {
+				return errors.Wrap(err, "could not delete block slot index")
+			}
+			if err = tx.Bucket(stateSlotIndicesBucket).Delete(bytesutil.SlotToBytesBigEndian(slot)); err != nil {
+				return errors.Wrap(err, "could not delete state slot index")
+			}
+		}
+
+		// Delete all caches after we have deleted everything from buckets.
+		// This is done after the buckets are deleted to avoid any issues in case of transaction rollback.
+		for _, root := range roots {
+			// Delete block from cache
+			s.blockCache.Del(string(root))
+			// Delete state summary from cache
+			s.stateSummaryCache.delete([32]byte(root))
+		}
+
+		return nil
+	})
+}
+
 // SaveBlock to the db.
 func (s *Store) SaveBlock(ctx context.Context, signed interfaces.ReadOnlySignedBeaconBlock) error {
 	ctx, span := trace.StartSpan(ctx, "BeaconDB.SaveBlock")
@@ -609,7 +689,7 @@ func blockRootsByFilter(ctx context.Context, tx *bolt.Tx, f *filters.QueryFilter

 	// We retrieve block roots that match a filter criteria of slot ranges, if specified.
 	filtersMap := f.Filters()
-	rootsBySlotRange, err := blockRootsBySlotRange(
+	rootsBySlotRange, _, err := blockRootsBySlotRange(
 		ctx,
 		tx.Bucket(blockSlotIndicesBucket),
 		filtersMap[filters.StartSlot],
@@ -627,6 +707,7 @@ func blockRootsByFilter(ctx context.Context, tx *bolt.Tx, f *filters.QueryFilter
 	// that list of roots to lookup the block. These block will
 	// meet the filter criteria.
 	indices := lookupValuesForIndices(ctx, indicesByBucket, tx)
+
 	keys := rootsBySlotRange
 	if len(indices) > 0 {
 		// If we have found indices that meet the filter criteria, and there are also
@@ -653,13 +734,13 @@ func blockRootsBySlotRange(
 	ctx context.Context,
 	bkt *bolt.Bucket,
 	startSlotEncoded, endSlotEncoded, startEpochEncoded, endEpochEncoded, slotStepEncoded interface{},
-) ([][]byte, error) {
+) ([][]byte, []primitives.Slot, error) {
 	_, span := trace.StartSpan(ctx, "BeaconDB.blockRootsBySlotRange")
 	defer span.End()

 	// Return nothing when all slot parameters are missing
 	if startSlotEncoded == nil && endSlotEncoded == nil && startEpochEncoded == nil && endEpochEncoded == nil {
-		return [][]byte{}, nil
+		return [][]byte{}, nil, nil
 	}

 	var startSlot, endSlot primitives.Slot
@@ -680,11 +761,11 @@ func blockRootsBySlotRange(
 	if startEpochOk && endEpochOk {
 		startSlot, err = slots.EpochStart(startEpoch)
 		if err != nil {
-			return nil, err
+			return nil, nil, err
 		}
 		endSlot, err = slots.EpochStart(endEpoch)
 		if err != nil {
-			return nil, err
+			return nil, nil, err
 		}
 		endSlot = endSlot + params.BeaconConfig().SlotsPerEpoch - 1
 	}
@@ -695,14 +776,15 @@ func blockRootsBySlotRange(
 		return key != nil && bytes.Compare(key, max) <= 0
 	}
 	if endSlot < startSlot {
-		return nil, errInvalidSlotRange
+		return nil, nil, errInvalidSlotRange
 	}
 	rootsRange := endSlot.SubSlot(startSlot).Div(step)
 	roots := make([][]byte, 0, rootsRange)
+	var slts []primitives.Slot
 	c := bkt.Cursor()
 	for k, v := c.Seek(min); conditional(k, max); k, v = c.Next() {
+		slot := bytesutil.BytesToSlotBigEndian(k)
 		if step > 1 {
-			slot := bytesutil.BytesToSlotBigEndian(k)
 			if slot.SubSlot(startSlot).Mod(step) != 0 {
 				continue
 			}
@@ -713,8 +795,9 @@ func blockRootsBySlotRange(
 			splitRoots = append(splitRoots, v[i:i+32])
 		}
 		roots = append(roots, splitRoots...)
+		slts = append(slts, slot)
 	}
-	return roots, nil
+	return roots, slts, nil
 }

 // blockRootsBySlot retrieves the block roots by slot
@@ -813,9 +896,9 @@ func unmarshalBlock(_ context.Context, enc []byte) (interfaces.ReadOnlySignedBea
 		if err := rawBlock.UnmarshalSSZ(enc[len(denebBlindKey):]); err != nil {
 			return nil, errors.Wrap(err, "could not unmarshal blinded Deneb block")
 		}
-	case hasElectraKey(enc):
+	case HasElectraKey(enc):
 		rawBlock = &ethpb.SignedBeaconBlockElectra{}
-		if err := rawBlock.UnmarshalSSZ(enc[len(electraKey):]); err != nil {
+		if err := rawBlock.UnmarshalSSZ(enc[len(ElectraKey):]); err != nil {
 			return nil, errors.Wrap(err, "could not unmarshal Electra block")
 		}
 	case hasElectraBlindKey(enc):
@@ -874,7 +957,7 @@ func keyForBlock(blk interfaces.ReadOnlySignedBeaconBlock) ([]byte, error) {
 		if blk.IsBlinded() {
 			return electraBlindKey, nil
 		}
-		return electraKey, nil
+		return ElectraKey, nil
 	}

 	if v >= version.Deneb {
@@ -908,3 +991,32 @@ func keyForBlock(blk interfaces.ReadOnlySignedBeaconBlock) ([]byte, error) {

 	return nil, fmt.Errorf("unsupported block version: %v", blk.Version())
 }
+
+func (s *Store) deleteBlock(tx *bolt.Tx, root []byte) error {
+	if err := tx.Bucket(blocksBucket).Delete(root); err != nil {
+		return errors.Wrap(err, "could not delete block")
+	}
+
+	if err := tx.Bucket(blockParentRootIndicesBucket).Delete(root); err != nil {
+		return errors.Wrap(err, "could not delete block parent indices")
+	}
+
+	return nil
+}
+
+func (s *Store) deleteValidatorHashes(tx *bolt.Tx, root []byte) error {
+	ok, err := s.isStateValidatorMigrationOver()
+	if err != nil {
+		return err
+	}
+	if !ok {
+		return nil
+	}
+
+	// Delete the validator hash index
+	if err = tx.Bucket(blockRootValidatorHashesBucket).Delete(root); err != nil {
+		return errors.Wrap(err, "could not delete validator index")
+	}
+
+	return nil
+}
--- a/beacon-chain/db/kv/blocks_test.go
+++ b/beacon-chain/db/kv/blocks_test.go
@@ -2,12 +2,14 @@ package kv

 import (
 	"context"
+	"fmt"
 	"testing"
 	"time"

 	"github.com/ethereum/go-ethereum/common"
 	"github.com/pkg/errors"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db/filters"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/state"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/interfaces"
@@ -18,6 +20,7 @@ import (
 	"github.com/prysmaticlabs/prysm/v5/testing/assert"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	bolt "go.etcd.io/bbolt"
 	"google.golang.org/protobuf/proto"
 )

@@ -353,6 +356,189 @@ func TestStore_DeleteFinalizedBlock(t *testing.T) {
 	require.NoError(t, db.SaveFinalizedCheckpoint(ctx, cp))
 	require.ErrorIs(t, db.DeleteBlock(ctx, root), ErrDeleteJustifiedAndFinalized)
 }
+
+func TestStore_HistoricalDataBeforeSlot(t *testing.T) {
+	slotsPerEpoch := uint64(params.BeaconConfig().SlotsPerEpoch)
+	db := setupDB(t)
+	ctx := context.Background()
+
+	// Save genesis block root
+	require.NoError(t, db.SaveGenesisBlockRoot(ctx, genesisBlockRoot))
+
+	// Create and save blocks for 4 epochs
+	blks := makeBlocks(t, 0, slotsPerEpoch*4, genesisBlockRoot)
+	require.NoError(t, db.SaveBlocks(ctx, blks))
+
+	// Mark state validator migration as complete
+	err := db.db.Update(func(tx *bolt.Tx) error {
+		return tx.Bucket(migrationsBucket).Put(migrationStateValidatorsKey, migrationCompleted)
+	})
+	require.NoError(t, err)
+
+	migrated, err := db.isStateValidatorMigrationOver()
+	require.NoError(t, err)
+	require.Equal(t, true, migrated)
+
+	// Create state summaries and states for each block
+	ss := make([]*ethpb.StateSummary, len(blks))
+	states := make([]state.BeaconState, len(blks))
+
+	for i, blk := range blks {
+		slot := blk.Block().Slot()
+		r, err := blk.Block().HashTreeRoot()
+		require.NoError(t, err)
+
+		// Create and save state summary
+		ss[i] = &ethpb.StateSummary{
+			Slot: slot,
+			Root: r[:],
+		}
+
+		// Create and save state with validator entries
+		vals := make([]*ethpb.Validator, 2)
+		for j := range vals {
+			vals[j] = &ethpb.Validator{
+				PublicKey:             bytesutil.PadTo([]byte{byte(i*j + 1)}, 48),
+				WithdrawalCredentials: bytesutil.PadTo([]byte{byte(i*j + 2)}, 32),
+			}
+		}
+
+		st, err := util.NewBeaconState(func(state *ethpb.BeaconState) error {
+			state.Validators = vals
+			state.Slot = slot
+			return nil
+		})
+		require.NoError(t, err)
+		require.NoError(t, db.SaveState(ctx, st, r))
+		states[i] = st
+
+		// Verify validator entries are saved to db
+		valsActual, err := db.validatorEntries(ctx, r)
+		require.NoError(t, err)
+		for j, val := range valsActual {
+			require.DeepEqual(t, vals[j], val)
+		}
+	}
+	require.NoError(t, db.SaveStateSummaries(ctx, ss))
+
+	// Verify slot indices exist before deletion
+	err = db.db.View(func(tx *bolt.Tx) error {
+		blockSlotBkt := tx.Bucket(blockSlotIndicesBucket)
+		stateSlotBkt := tx.Bucket(stateSlotIndicesBucket)
+
+		for i := uint64(0); i < slotsPerEpoch; i++ {
+			slot := bytesutil.SlotToBytesBigEndian(primitives.Slot(i + 1))
+			assert.NotNil(t, blockSlotBkt.Get(slot), "Expected block slot index to exist")
+			assert.NotNil(t, stateSlotBkt.Get(slot), "Expected state slot index to exist", i)
+		}
+		return nil
+	})
+	require.NoError(t, err)
+
+	// Delete data before slot at epoch 1
+	require.NoError(t, db.DeleteHistoricalDataBeforeSlot(ctx, primitives.Slot(slotsPerEpoch)))
+
+	// Verify blocks from epoch 0 are deleted
+	for i := uint64(0); i < slotsPerEpoch; i++ {
+		root, err := blks[i].Block().HashTreeRoot()
+		require.NoError(t, err)
+
+		// Check block is deleted
+		retrievedBlocks, err := db.BlocksBySlot(ctx, primitives.Slot(i))
+		require.NoError(t, err)
+		assert.Equal(t, 0, len(retrievedBlocks))
+
+		// Verify block does not exist
+		assert.Equal(t, false, db.HasBlock(ctx, root))
+
+		// Verify block parent root does not exist
+		err = db.db.View(func(tx *bolt.Tx) error {
+			require.Equal(t, 0, len(tx.Bucket(blockParentRootIndicesBucket).Get(root[:])))
+			return nil
+		})
+		require.NoError(t, err)
+
+		// Verify state is deleted
+		hasState := db.HasState(ctx, root)
+		assert.Equal(t, false, hasState)
+
+		// Verify state summary is deleted
+		hasSummary := db.HasStateSummary(ctx, root)
+		assert.Equal(t, false, hasSummary)
+
+		// Verify validator hashes for block roots are deleted
+		err = db.db.View(func(tx *bolt.Tx) error {
+			assert.Equal(t, 0, len(tx.Bucket(blockRootValidatorHashesBucket).Get(root[:])))
+			return nil
+		})
+		require.NoError(t, err)
+	}
+
+	// Verify slot indices are deleted
+	err = db.db.View(func(tx *bolt.Tx) error {
+		blockSlotBkt := tx.Bucket(blockSlotIndicesBucket)
+		stateSlotBkt := tx.Bucket(stateSlotIndicesBucket)
+
+		for i := uint64(0); i < slotsPerEpoch; i++ {
+			slot := bytesutil.SlotToBytesBigEndian(primitives.Slot(i + 1))
+			assert.Equal(t, 0, len(blockSlotBkt.Get(slot)), fmt.Sprintf("Expected block slot index to be deleted, slot: %d", slot))
+			assert.Equal(t, 0, len(stateSlotBkt.Get(slot)), fmt.Sprintf("Expected state slot index to be deleted, slot: %d", slot))
+		}
+		return nil
+	})
+	require.NoError(t, err)
+
+	// Verify blocks from epochs 1-3 still exist
+	for i := slotsPerEpoch; i < slotsPerEpoch*4; i++ {
+		root, err := blks[i].Block().HashTreeRoot()
+		require.NoError(t, err)
+
+		// Verify block exists
+		assert.Equal(t, true, db.HasBlock(ctx, root))
+
+		// Verify remaining block parent root exists, except last slot since we store parent roots of each block.
+		if i < slotsPerEpoch*4-1 {
+			err = db.db.View(func(tx *bolt.Tx) error {
+				require.NotNil(t, tx.Bucket(blockParentRootIndicesBucket).Get(root[:]), fmt.Sprintf("Expected block parent index to be deleted, slot: %d", i))
+				return nil
+			})
+			require.NoError(t, err)
+		}
+
+		// Verify state exists
+		hasState := db.HasState(ctx, root)
+		assert.Equal(t, true, hasState)
+
+		// Verify state summary exists
+		hasSummary := db.HasStateSummary(ctx, root)
+		assert.Equal(t, true, hasSummary)
+
+		// Verify slot indices still exist
+		err = db.db.View(func(tx *bolt.Tx) error {
+			blockSlotBkt := tx.Bucket(blockSlotIndicesBucket)
+			stateSlotBkt := tx.Bucket(stateSlotIndicesBucket)
+
+			slot := bytesutil.SlotToBytesBigEndian(primitives.Slot(i + 1))
+			assert.NotNil(t, blockSlotBkt.Get(slot), "Expected block slot index to exist")
+			assert.NotNil(t, stateSlotBkt.Get(slot), "Expected state slot index to exist")
+			return nil
+		})
+		require.NoError(t, err)
+
+		// Verify validator entries still exist
+		valsActual, err := db.validatorEntries(ctx, root)
+		require.NoError(t, err)
+		assert.NotNil(t, valsActual)
+
+		// Verify remaining validator hashes for block roots exists
+		err = db.db.View(func(tx *bolt.Tx) error {
+			assert.NotNil(t, tx.Bucket(blockRootValidatorHashesBucket).Get(root[:]))
+			return nil
+		})
+		require.NoError(t, err)
+	}
+}
+
 func TestStore_GenesisBlock(t *testing.T) {
 	db := setupDB(t)
 	ctx := context.Background()
--- a/beacon-chain/db/kv/key.go
+++ b/beacon-chain/db/kv/key.go
@@ -52,11 +52,12 @@ func hasDenebBlindKey(enc []byte) bool {
 	return bytes.Equal(enc[:len(denebBlindKey)], denebBlindKey)
 }

-func hasElectraKey(enc []byte) bool {
-	if len(electraKey) >= len(enc) {
+// HasElectraKey verifies if the encoding is Electra compatible.
+func HasElectraKey(enc []byte) bool {
+	if len(ElectraKey) >= len(enc) {
 		return false
 	}
-	return bytes.Equal(enc[:len(electraKey)], electraKey)
+	return bytes.Equal(enc[:len(ElectraKey)], ElectraKey)
 }

 func hasElectraBlindKey(enc []byte) bool {
--- a/beacon-chain/db/kv/lightclient.go
+++ b/beacon-chain/db/kv/lightclient.go
@@ -167,13 +167,13 @@ func decodeLightClientBootstrap(enc []byte) (interfaces.LightClientBootstrap, []
 		}
 		m = bootstrap
 		syncCommitteeHash = enc[len(denebKey) : len(denebKey)+32]
-	case hasElectraKey(enc):
+	case HasElectraKey(enc):
 		bootstrap := &ethpb.LightClientBootstrapElectra{}
-		if err := bootstrap.UnmarshalSSZ(enc[len(electraKey)+32:]); err != nil {
+		if err := bootstrap.UnmarshalSSZ(enc[len(ElectraKey)+32:]); err != nil {
 			return nil, nil, errors.Wrap(err, "could not unmarshal Electra light client bootstrap")
 		}
 		m = bootstrap
-		syncCommitteeHash = enc[len(electraKey) : len(electraKey)+32]
+		syncCommitteeHash = enc[len(ElectraKey) : len(ElectraKey)+32]
 	default:
 		return nil, nil, errors.New("decoding of saved light client bootstrap is unsupported")
 	}
@@ -277,9 +277,9 @@ func decodeLightClientUpdate(enc []byte) (interfaces.LightClientUpdate, error) {
 			return nil, errors.Wrap(err, "could not unmarshal Deneb light client update")
 		}
 		m = update
-	case hasElectraKey(enc):
+	case HasElectraKey(enc):
 		update := &ethpb.LightClientUpdateElectra{}
-		if err := update.UnmarshalSSZ(enc[len(electraKey):]); err != nil {
+		if err := update.UnmarshalSSZ(enc[len(ElectraKey):]); err != nil {
 			return nil, errors.Wrap(err, "could not unmarshal Electra light client update")
 		}
 		m = update
@@ -292,7 +292,7 @@ func decodeLightClientUpdate(enc []byte) (interfaces.LightClientUpdate, error) {
 func keyForLightClientUpdate(v int) ([]byte, error) {
 	switch v {
 	case version.Electra:
-		return electraKey, nil
+		return ElectraKey, nil
 	case version.Deneb:
 		return denebKey, nil
 	case version.Capella:
--- a/beacon-chain/db/kv/schema.go
+++ b/beacon-chain/db/kv/schema.go
@@ -53,7 +53,7 @@ var (
 	saveBlindedBeaconBlocksKey = []byte("save-blinded-beacon-blocks")
 	denebKey                   = []byte("deneb")
 	denebBlindKey              = []byte("blind-deneb")
-	electraKey                 = []byte("electra")
+	ElectraKey                 = []byte("electra")
 	electraBlindKey            = []byte("blind-electra")
 	fuluKey                    = []byte("fulu")
 	fuluBlindKey               = []byte("blind-fulu")
--- a/beacon-chain/db/kv/state.go
+++ b/beacon-chain/db/kv/state.go
@@ -357,7 +357,7 @@ func (s *Store) processElectra(ctx context.Context, pbState *ethpb.BeaconStateEl
 	if err != nil {
 		return err
 	}
-	encodedState := snappy.Encode(nil, append(electraKey, rawObj...))
+	encodedState := snappy.Encode(nil, append(ElectraKey, rawObj...))
 	if err := bucket.Put(rootHash, encodedState); err != nil {
 		return err
 	}
@@ -530,9 +530,9 @@ func (s *Store) unmarshalState(_ context.Context, enc []byte, validatorEntries [
 			protoState.Validators = validatorEntries
 		}
 		return statenative.InitializeFromProtoUnsafeFulu(protoState)
-	case hasElectraKey(enc):
+	case HasElectraKey(enc):
 		protoState := &ethpb.BeaconStateElectra{}
-		if err := protoState.UnmarshalSSZ(enc[len(electraKey):]); err != nil {
+		if err := protoState.UnmarshalSSZ(enc[len(ElectraKey):]); err != nil {
 			return nil, errors.Wrap(err, "failed to unmarshal encoding for Electra")
 		}
 		ok, err := s.isStateValidatorMigrationOver()
@@ -688,7 +688,7 @@ func marshalState(ctx context.Context, st state.ReadOnlyBeaconState) ([]byte, er
 		if err != nil {
 			return nil, err
 		}
-		return snappy.Encode(nil, append(electraKey, rawObj...)), nil
+		return snappy.Encode(nil, append(ElectraKey, rawObj...)), nil
 	case version.Fulu:
 		rState, ok := st.ToProtoUnsafe().(*ethpb.BeaconStateFulu)
 		if !ok {
@@ -725,7 +725,7 @@ func (s *Store) validatorEntries(ctx context.Context, blockRoot [32]byte) ([]*et
 		idxBkt := tx.Bucket(blockRootValidatorHashesBucket)
 		valKey := idxBkt.Get(blockRoot[:])
 		if len(valKey) == 0 {
-			return errors.Errorf("invalid compressed validator keys length")
+			return errors.Errorf("validator keys not found for given block root: %x", blockRoot)
 		}

 		// decompress the keys and check if they are of proper length.
--- a/beacon-chain/db/pruner/BUILD.bazel
+++ b/beacon-chain/db/pruner/BUILD.bazel
@@ -0,0 +1,38 @@
+load("@prysm//tools/go:def.bzl", "go_library", "go_test")
+
+go_library(
+    name = "go_default_library",
+    srcs = ["pruner.go"],
+    importpath = "github.com/prysmaticlabs/prysm/v5/beacon-chain/db/pruner",
+    visibility = [
+        "//beacon-chain:__subpackages__",
+    ],
+    deps = [
+        "//beacon-chain/core/helpers:go_default_library",
+        "//beacon-chain/db:go_default_library",
+        "//beacon-chain/db/iface:go_default_library",
+        "//config/params:go_default_library",
+        "//consensus-types/primitives:go_default_library",
+        "//time/slots:go_default_library",
+        "@com_github_pkg_errors//:go_default_library",
+        "@com_github_sirupsen_logrus//:go_default_library",
+    ],
+)
+
+go_test(
+    name = "go_default_test",
+    srcs = ["pruner_test.go"],
+    embed = [":go_default_library"],
+    deps = [
+        "//beacon-chain/db/testing:go_default_library",
+        "//config/params:go_default_library",
+        "//consensus-types/blocks:go_default_library",
+        "//consensus-types/primitives:go_default_library",
+        "//proto/prysm/v1alpha1:go_default_library",
+        "//testing/require:go_default_library",
+        "//testing/util:go_default_library",
+        "//time/slots/testing:go_default_library",
+        "@com_github_sirupsen_logrus//:go_default_library",
+        "@com_github_sirupsen_logrus//hooks/test:go_default_library",
+    ],
+)
--- a/beacon-chain/db/pruner/pruner.go
+++ b/beacon-chain/db/pruner/pruner.go
@@ -0,0 +1,174 @@
+package pruner
+
+import (
+	"context"
+	"time"
+
+	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/core/helpers"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db/iface"
+	"github.com/prysmaticlabs/prysm/v5/config/params"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/time/slots"
+	"github.com/sirupsen/logrus"
+)
+
+var log = logrus.WithField("prefix", "db-pruner")
+
+type ServiceOption func(*Service)
+
+// WithRetentionPeriod allows the user to specify a different data retention period than the spec default.
+// The retention period is specified in epochs, and must be >= MIN_EPOCHS_FOR_BLOCK_REQUESTS.
+func WithRetentionPeriod(retentionEpochs primitives.Epoch) ServiceOption {
+	return func(s *Service) {
+		defaultRetentionEpochs := helpers.MinEpochsForBlockRequests() + 1
+		if retentionEpochs < defaultRetentionEpochs {
+			log.WithField("userEpochs", retentionEpochs).
+				WithField("minRequired", defaultRetentionEpochs).
+				Warn("Retention period too low, using minimum required value")
+		}
+
+		s.ps = pruneStartSlotFunc(retentionEpochs)
+	}
+}
+
+func WithSlotTicker(slotTicker slots.Ticker) ServiceOption {
+	return func(s *Service) {
+		s.slotTicker = slotTicker
+	}
+}
+
+// Service defines a service that prunes beacon chain DB based on MIN_EPOCHS_FOR_BLOCK_REQUESTS.
+type Service struct {
+	ctx            context.Context
+	db             db.Database
+	ps             func(current primitives.Slot) primitives.Slot
+	prunedUpto     primitives.Slot
+	done           chan struct{}
+	slotTicker     slots.Ticker
+	backfillWaiter func() error
+	initSyncWaiter func() error
+}
+
+func New(ctx context.Context, db iface.Database, genesisTime uint64, initSyncWaiter, backfillWaiter func() error, opts ...ServiceOption) (*Service, error) {
+	p := &Service{
+		ctx:            ctx,
+		db:             db,
+		ps:             pruneStartSlotFunc(helpers.MinEpochsForBlockRequests() + 1), // Default retention epochs is MIN_EPOCHS_FOR_BLOCK_REQUESTS + 1 from the current slot.
+		done:           make(chan struct{}),
+		slotTicker:     slots.NewSlotTicker(slots.StartTime(genesisTime, 0), params.BeaconConfig().SecondsPerSlot),
+		initSyncWaiter: initSyncWaiter,
+		backfillWaiter: backfillWaiter,
+	}
+
+	for _, o := range opts {
+		o(p)
+	}
+
+	return p, nil
+}
+
+func (p *Service) Start() {
+	log.Info("Starting Beacon DB pruner service")
+	p.run()
+}
+
+func (p *Service) Stop() error {
+	log.Info("Stopping Beacon DB pruner service")
+	close(p.done)
+	return nil
+}
+
+func (p *Service) Status() error {
+	return nil
+}
+
+func (p *Service) run() {
+	if p.initSyncWaiter != nil {
+		log.Info("Waiting for initial sync service to complete before starting pruner")
+		if err := p.initSyncWaiter(); err != nil {
+			log.WithError(err).Error("Failed to start database pruner, error waiting for initial sync completion")
+			return
+		}
+	}
+	if p.backfillWaiter != nil {
+		log.Info("Waiting for backfill service to complete before starting pruner")
+		if err := p.backfillWaiter(); err != nil {
+			log.WithError(err).Error("Failed to start database pruner, error waiting for backfill completion")
+			return
+		}
+	}
+
+	defer p.slotTicker.Done()
+
+	for {
+		select {
+		case <-p.ctx.Done():
+			log.Debug("Stopping Beacon DB pruner service", "prunedUpto", p.prunedUpto)
+			return
+		case <-p.done:
+			log.Debug("Stopping Beacon DB pruner service", "prunedUpto", p.prunedUpto)
+			return
+		case slot := <-p.slotTicker.C():
+			// Prune at the middle of every epoch since we do a lot of things around epoch boundaries.
+			if slots.SinceEpochStarts(slot) != (params.BeaconConfig().SlotsPerEpoch / 2) {
+				continue
+			}
+
+			if err := p.prune(slot); err != nil {
+				log.WithError(err).Error("Failed to prune database")
+			}
+		}
+	}
+}
+
+// prune deletes historical chain data beyond the pruneSlot.
+func (p *Service) prune(slot primitives.Slot) error {
+	// Prune everything up to this slot (inclusive).
+	pruneUpto := p.ps(slot)
+
+	// Can't prune beyond genesis.
+	if pruneUpto == 0 {
+		return nil
+	}
+
+	// Skip if already pruned up to this slot.
+	if pruneUpto <= p.prunedUpto {
+		return nil
+	}
+
+	log.WithFields(logrus.Fields{
+		"pruneUpto": pruneUpto,
+	}).Debug("Pruning chain data")
+
+	tt := time.Now()
+	if err := p.db.DeleteHistoricalDataBeforeSlot(p.ctx, pruneUpto); err != nil {
+		return errors.Wrapf(err, "could not delete upto slot %d", pruneUpto)
+	}
+
+	log.WithFields(logrus.Fields{
+		"prunedUpto":  pruneUpto,
+		"duration":    time.Since(tt),
+		"currentSlot": slot,
+	}).Debug("Successfully pruned chain data")
+
+	// Update pruning checkpoint.
+	p.prunedUpto = pruneUpto
+
+	return nil
+}
+
+// pruneStartSlotFunc returns the function to determine the start slot to start pruning.
+func pruneStartSlotFunc(retentionEpochs primitives.Epoch) func(primitives.Slot) primitives.Slot {
+	return func(current primitives.Slot) primitives.Slot {
+		if retentionEpochs > slots.MaxSafeEpoch() {
+			retentionEpochs = slots.MaxSafeEpoch()
+		}
+		offset := slots.UnsafeEpochStart(retentionEpochs)
+		if offset >= current {
+			return 0
+		}
+		return current - offset
+	}
+}
--- a/beacon-chain/db/pruner/pruner_test.go
+++ b/beacon-chain/db/pruner/pruner_test.go
@@ -0,0 +1,135 @@
+package pruner
+
+import (
+	"context"
+	"testing"
+	"time"
+
+	"github.com/prysmaticlabs/prysm/v5/config/params"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/blocks"
+	eth "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+
+	"github.com/prysmaticlabs/prysm/v5/testing/util"
+	slottest "github.com/prysmaticlabs/prysm/v5/time/slots/testing"
+	"github.com/sirupsen/logrus"
+
+	dbtest "github.com/prysmaticlabs/prysm/v5/beacon-chain/db/testing"
+	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/testing/require"
+	logTest "github.com/sirupsen/logrus/hooks/test"
+)
+
+func TestPruner_PruningConditions(t *testing.T) {
+	tests := []struct {
+		name              string
+		synced            bool
+		backfillCompleted bool
+		expectedLog       string
+	}{
+		{
+			name:              "Not synced",
+			synced:            false,
+			backfillCompleted: true,
+			expectedLog:       "Waiting for initial sync service to complete before starting pruner",
+		},
+		{
+			name:              "Backfill incomplete",
+			synced:            true,
+			backfillCompleted: false,
+			expectedLog:       "Waiting for backfill service to complete before starting pruner",
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			logrus.SetLevel(logrus.DebugLevel)
+			hook := logTest.NewGlobal()
+			ctx, cancel := context.WithCancel(context.Background())
+			beaconDB := dbtest.SetupDB(t)
+
+			slotTicker := &slottest.MockTicker{Channel: make(chan primitives.Slot)}
+
+			waitChan := make(chan struct{})
+			waiter := func() error {
+				close(waitChan)
+				return nil
+			}
+
+			var initSyncWaiter, backfillWaiter func() error
+			if !tt.synced {
+				initSyncWaiter = waiter
+			}
+			if !tt.backfillCompleted {
+				backfillWaiter = waiter
+			}
+			p, err := New(ctx, beaconDB, uint64(time.Now().Unix()), initSyncWaiter, backfillWaiter, WithSlotTicker(slotTicker))
+			require.NoError(t, err)
+
+			go p.Start()
+			<-waitChan
+			cancel()
+
+			if tt.expectedLog != "" {
+				require.LogsContain(t, hook, tt.expectedLog)
+			}
+
+			require.NoError(t, p.Stop())
+		})
+	}
+}
+
+func TestPruner_PruneSuccess(t *testing.T) {
+	ctx := context.Background()
+	beaconDB := dbtest.SetupDB(t)
+
+	// Create and save some blocks at different slots
+	var blks []*eth.SignedBeaconBlock
+	for slot := primitives.Slot(1); slot <= 32; slot++ {
+		blk := util.NewBeaconBlock()
+		blk.Block.Slot = slot
+		wsb, err := blocks.NewSignedBeaconBlock(blk)
+		require.NoError(t, err)
+		require.NoError(t, beaconDB.SaveBlock(ctx, wsb))
+		blks = append(blks, blk)
+	}
+
+	// Create pruner with retention of 2 epochs (64 slots)
+	retentionEpochs := primitives.Epoch(2)
+	slotTicker := &slottest.MockTicker{Channel: make(chan primitives.Slot)}
+
+	p, err := New(
+		ctx,
+		beaconDB,
+		uint64(time.Now().Unix()),
+		nil,
+		nil,
+		WithSlotTicker(slotTicker),
+	)
+	require.NoError(t, err)
+
+	p.ps = func(current primitives.Slot) primitives.Slot {
+		return current - primitives.Slot(retentionEpochs)*params.BeaconConfig().SlotsPerEpoch
+	}
+
+	// Start pruner and trigger at middle of 3rd epoch (slot 80)
+	go p.Start()
+	currentSlot := primitives.Slot(80) // Middle of 3rd epoch
+	slotTicker.Channel <- currentSlot
+	// Send the same slot again to ensure the pruning operation completes
+	slotTicker.Channel <- currentSlot
+
+	for slot := primitives.Slot(1); slot <= 32; slot++ {
+		root, err := blks[slot-1].Block.HashTreeRoot()
+		require.NoError(t, err)
+		present := beaconDB.HasBlock(ctx, root)
+		if slot <= 16 { // These should be pruned
+			require.NoError(t, err)
+			require.Equal(t, false, present, "Expected present at slot %d to be pruned", slot)
+		} else { // These should remain
+			require.NoError(t, err)
+			require.Equal(t, true, present, "Expected present at slot %d to exist", slot)
+		}
+	}
+
+	require.NoError(t, p.Stop())
+}
--- a/beacon-chain/db/slasherkv/BUILD.bazel
+++ b/beacon-chain/db/slasherkv/BUILD.bazel
@@ -15,6 +15,7 @@ go_library(
    visibility = ["//beacon-chain:__subpackages__"],
    deps = [
        "//beacon-chain/db/iface:go_default_library",
+        "//beacon-chain/db/kv:go_default_library",
        "//beacon-chain/slasher/types:go_default_library",
        "//config/params:go_default_library",
        "//consensus-types/primitives:go_default_library",
@@ -22,6 +23,7 @@ go_library(
        "//io/file:go_default_library",
        "//monitoring/tracing/trace:go_default_library",
        "//proto/prysm/v1alpha1:go_default_library",
+        "//runtime/version:go_default_library",
        "//time/slots:go_default_library",
        "@com_github_golang_snappy//:go_default_library",
        "@com_github_pkg_errors//:go_default_library",
@@ -50,6 +52,7 @@ go_test(
        "//consensus-types/primitives:go_default_library",
        "//encoding/bytesutil:go_default_library",
        "//proto/prysm/v1alpha1:go_default_library",
+        "//runtime/version:go_default_library",
        "//testing/require:go_default_library",
        "//time/slots:go_default_library",
        "@com_github_prysmaticlabs_fastssz//:go_default_library",
--- a/beacon-chain/db/slasherkv/pruning_test.go
+++ b/beacon-chain/db/slasherkv/pruning_test.go
@@ -8,6 +8,7 @@ import (
 	slashertypes "github.com/prysmaticlabs/prysm/v5/beacon-chain/slasher/types"
 	"github.com/prysmaticlabs/prysm/v5/config/params"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
+	"github.com/prysmaticlabs/prysm/v5/runtime/version"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 	"github.com/prysmaticlabs/prysm/v5/time/slots"
 	logTest "github.com/sirupsen/logrus/hooks/test"
@@ -177,8 +178,8 @@ func TestStore_PruneAttestations_OK(t *testing.T) {
 				if i > 0 {
 					source = target - 1
 				}
-				att1 := createAttestationWrapper(source, target, []uint64{attester1}, []byte{0})
-				att2 := createAttestationWrapper(source, target, []uint64{attester2}, []byte{1})
+				att1 := createAttestationWrapper(version.Phase0, source, target, []uint64{attester1}, []byte{0})
+				att2 := createAttestationWrapper(version.Phase0, source, target, []uint64{attester2}, []byte{1})
 				attestations = append(attestations, att1, att2)
 			}
 		}
--- a/beacon-chain/db/slasherkv/slasher.go
+++ b/beacon-chain/db/slasherkv/slasher.go
@@ -11,11 +11,13 @@ import (
 	"github.com/golang/snappy"
 	"github.com/pkg/errors"
 	ssz "github.com/prysmaticlabs/fastssz"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db/kv"
 	slashertypes "github.com/prysmaticlabs/prysm/v5/beacon-chain/slasher/types"
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	"github.com/prysmaticlabs/prysm/v5/monitoring/tracing/trace"
 	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+	"github.com/prysmaticlabs/prysm/v5/runtime/version"
 	bolt "go.etcd.io/bbolt"
 	"golang.org/x/sync/errgroup"
 )
@@ -692,6 +694,11 @@ func encodeAttestationRecord(att *slashertypes.IndexedAttestationWrapper) ([]byt
 		return []byte{}, errors.New("nil proposal record")
 	}

+	var versionKey []byte
+	if att.IndexedAttestation.Version() >= version.Electra {
+		versionKey = kv.ElectraKey
+	}
+
 	// Encode attestation.
 	encodedAtt, err := att.IndexedAttestation.MarshalSSZ()
 	if err != nil {
@@ -701,7 +708,14 @@ func encodeAttestationRecord(att *slashertypes.IndexedAttestationWrapper) ([]byt
 	// Compress attestation.
 	compressedAtt := snappy.Encode(nil, encodedAtt)

-	return append(att.DataRoot[:], compressedAtt...), nil
+	enc := make([]byte, len(versionKey)+len(att.DataRoot)+len(compressedAtt))
+	if len(versionKey) > 0 {
+		copy(enc, versionKey)
+	}
+	copy(enc[len(versionKey):len(versionKey)+len(att.DataRoot)], att.DataRoot[:])
+	copy(enc[len(versionKey)+len(att.DataRoot):], compressedAtt)
+
+	return enc, nil
 }

 // Decode attestation record from bytes.
@@ -711,6 +725,11 @@ func decodeAttestationRecord(encoded []byte) (*slashertypes.IndexedAttestationWr
 		return nil, fmt.Errorf("wrong length for encoded attestation record, want minimum %d, got %d", rootSize, len(encoded))
 	}

+	postElectra := kv.HasElectraKey(encoded)
+	if postElectra {
+		encoded = encoded[len(kv.ElectraKey):]
+	}
+
 	// Decompress attestation.
 	decodedAttBytes, err := snappy.Decode(nil, encoded[rootSize:])
 	if err != nil {
@@ -718,8 +737,14 @@ func decodeAttestationRecord(encoded []byte) (*slashertypes.IndexedAttestationWr
 	}

 	// Decode attestation.
-	decodedAtt := &ethpb.IndexedAttestation{}
-	if err := decodedAtt.UnmarshalSSZ(decodedAttBytes); err != nil {
+	var decodedAtt ethpb.IndexedAtt
+	if postElectra {
+		decodedAtt = &ethpb.IndexedAttestationElectra{}
+	} else {
+		decodedAtt = &ethpb.IndexedAttestation{}
+	}
+
+	if err = decodedAtt.UnmarshalSSZ(decodedAttBytes); err != nil {
 		return nil, err
 	}

--- a/beacon-chain/db/slasherkv/slasher_test.go
+++ b/beacon-chain/db/slasherkv/slasher_test.go
@@ -14,20 +14,16 @@ import (
 	"github.com/prysmaticlabs/prysm/v5/consensus-types/primitives"
 	"github.com/prysmaticlabs/prysm/v5/encoding/bytesutil"
 	ethpb "github.com/prysmaticlabs/prysm/v5/proto/prysm/v1alpha1"
+	"github.com/prysmaticlabs/prysm/v5/runtime/version"
 	"github.com/prysmaticlabs/prysm/v5/testing/require"
 )

 func TestStore_AttestationRecordForValidator_SaveRetrieve(t *testing.T) {
 	const attestationsCount = 11_000
-
-	// Create context.
 	ctx := context.Background()
-
-	// Create database.
 	beaconDB := setupDB(t)
-
-	// Define the validator index.
-	validatorIndex := primitives.ValidatorIndex(1)
+	phase0ValidatorIndex := primitives.ValidatorIndex(1)
+	electraValidatorIndex := primitives.ValidatorIndex(2)

 	// Defines attestations to save and retrieve.
 	attWrappers := make([]*slashertypes.IndexedAttestationWrapper, attestationsCount)
@@ -36,33 +32,71 @@ func TestStore_AttestationRecordForValidator_SaveRetrieve(t *testing.T) {
 		binary.LittleEndian.PutUint64(dataRoot[:], uint64(i))

 		attWrapper := createAttestationWrapper(
+			version.Phase0,
 			primitives.Epoch(i),
 			primitives.Epoch(i+1),
-			[]uint64{uint64(validatorIndex)},
+			[]uint64{uint64(phase0ValidatorIndex)},
 			dataRoot[:],
 		)

 		attWrappers[i] = attWrapper
 	}
+	attWrappersElectra := make([]*slashertypes.IndexedAttestationWrapper, attestationsCount)
+	for i := 0; i < attestationsCount; i++ {
+		var dataRoot [32]byte
+		binary.LittleEndian.PutUint64(dataRoot[:], uint64(i))

-	// Check on a sample of validators that no attestation records are available.
-	for i := 0; i < attestationsCount; i += 100 {
-		attRecord, err := beaconDB.AttestationRecordForValidator(ctx, validatorIndex, primitives.Epoch(i+1))
-		require.NoError(t, err)
-		require.Equal(t, true, attRecord == nil)
+		attWrapper := createAttestationWrapper(
+			version.Electra,
+			primitives.Epoch(i),
+			primitives.Epoch(i+1),
+			[]uint64{uint64(electraValidatorIndex)},
+			dataRoot[:],
+		)
+
+		attWrappersElectra[i] = attWrapper
 	}

-	// Save the attestation records to the database.
-	err := beaconDB.SaveAttestationRecordsForValidators(ctx, attWrappers)
-	require.NoError(t, err)
+	type testCase struct {
+		name string
+		atts []*slashertypes.IndexedAttestationWrapper
+		vi   primitives.ValidatorIndex
+	}
+	testCases := []testCase{
+		{
+			name: "phase0",
+			atts: attWrappers,
+			vi:   phase0ValidatorIndex,
+		},
+		{
+			name: "electra",
+			atts: attWrappersElectra,
+			vi:   electraValidatorIndex,
+		},
+	}

-	// Check on a sample of validators that attestation records are available.
-	for i := 0; i < attestationsCount; i += 100 {
-		expected := attWrappers[i]
-		actual, err := beaconDB.AttestationRecordForValidator(ctx, validatorIndex, primitives.Epoch(i+1))
-		require.NoError(t, err)
+	for _, tc := range testCases {
+		t.Run(tc.name, func(t *testing.T) {
+			// Check on a sample of validators that no attestation records are available.
+			for i := 0; i < attestationsCount; i += 100 {
+				attRecord, err := beaconDB.AttestationRecordForValidator(ctx, tc.vi, primitives.Epoch(i+1))
+				require.NoError(t, err)
+				require.Equal(t, true, attRecord == nil)
+			}

-		require.DeepEqual(t, expected.IndexedAttestation.GetData().Source.Epoch, actual.IndexedAttestation.GetData().Source.Epoch)
+			// Save the attestation records to the database.
+			err := beaconDB.SaveAttestationRecordsForValidators(ctx, tc.atts)
+			require.NoError(t, err)
+
+			// Check on a sample of validators that attestation records are available.
+			for i := 0; i < attestationsCount; i += 100 {
+				expected := attWrappers[i]
+				actual, err := beaconDB.AttestationRecordForValidator(ctx, tc.vi, primitives.Epoch(i+1))
+				require.NoError(t, err)
+
+				require.DeepEqual(t, expected.IndexedAttestation.GetData().Source.Epoch, actual.IndexedAttestation.GetData().Source.Epoch)
+			}
+		})
 	}
 }

@@ -108,55 +142,60 @@ func TestStore_LastEpochWrittenForValidators(t *testing.T) {

 func TestStore_CheckAttesterDoubleVotes(t *testing.T) {
 	ctx := context.Background()
-	beaconDB := setupDB(t)
-	err := beaconDB.SaveAttestationRecordsForValidators(ctx, []*slashertypes.IndexedAttestationWrapper{
-		createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{1}),
-		createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{3}),
-	})
-	require.NoError(t, err)

-	slashableAtts := []*slashertypes.IndexedAttestationWrapper{
-		createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{2}), // Different signing root.
-		createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{4}), // Different signing root.
-	}
+	for _, ver := range []int{version.Phase0, version.Electra} {
+		t.Run(version.String(ver), func(t *testing.T) {
+			beaconDB := setupDB(t)
+			err := beaconDB.SaveAttestationRecordsForValidators(ctx, []*slashertypes.IndexedAttestationWrapper{
+				createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{1}),
+				createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{3}),
+			})
+			require.NoError(t, err)

-	wanted := []*slashertypes.AttesterDoubleVote{
-		{
-			ValidatorIndex: 0,
-			Target:         3,
-			Wrapper_1:      createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{1}),
-			Wrapper_2:      createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{2}),
-		},
-		{
-			ValidatorIndex: 1,
-			Target:         3,
-			Wrapper_1:      createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{1}),
-			Wrapper_2:      createAttestationWrapper(2, 3, []uint64{0, 1}, []byte{2}),
-		},
-		{
-			ValidatorIndex: 2,
-			Target:         4,
-			Wrapper_1:      createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{3}),
-			Wrapper_2:      createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{4}),
-		},
-		{
-			ValidatorIndex: 3,
-			Target:         4,
-			Wrapper_1:      createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{3}),
-			Wrapper_2:      createAttestationWrapper(3, 4, []uint64{2, 3}, []byte{4}),
-		},
-	}
-	doubleVotes, err := beaconDB.CheckAttesterDoubleVotes(ctx, slashableAtts)
-	require.NoError(t, err)
-	sort.SliceStable(doubleVotes, func(i, j int) bool {
-		return uint64(doubleVotes[i].ValidatorIndex) < uint64(doubleVotes[j].ValidatorIndex)
-	})
-	require.Equal(t, len(wanted), len(doubleVotes))
-	for i, double := range doubleVotes {
-		require.DeepEqual(t, wanted[i].ValidatorIndex, double.ValidatorIndex)
-		require.DeepEqual(t, wanted[i].Target, double.Target)
-		require.DeepEqual(t, wanted[i].Wrapper_1, double.Wrapper_1)
-		require.DeepEqual(t, wanted[i].Wrapper_2, double.Wrapper_2)
+			slashableAtts := []*slashertypes.IndexedAttestationWrapper{
+				createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{2}), // Different signing root.
+				createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{4}), // Different signing root.
+			}
+
+			wanted := []*slashertypes.AttesterDoubleVote{
+				{
+					ValidatorIndex: 0,
+					Target:         3,
+					Wrapper_1:      createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{1}),
+					Wrapper_2:      createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{2}),
+				},
+				{
+					ValidatorIndex: 1,
+					Target:         3,
+					Wrapper_1:      createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{1}),
+					Wrapper_2:      createAttestationWrapper(version.Phase0, 2, 3, []uint64{0, 1}, []byte{2}),
+				},
+				{
+					ValidatorIndex: 2,
+					Target:         4,
+					Wrapper_1:      createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{3}),
+					Wrapper_2:      createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{4}),
+				},
+				{
+					ValidatorIndex: 3,
+					Target:         4,
+					Wrapper_1:      createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{3}),
+					Wrapper_2:      createAttestationWrapper(version.Phase0, 3, 4, []uint64{2, 3}, []byte{4}),
+				},
+			}
+			doubleVotes, err := beaconDB.CheckAttesterDoubleVotes(ctx, slashableAtts)
+			require.NoError(t, err)
+			sort.SliceStable(doubleVotes, func(i, j int) bool {
+				return uint64(doubleVotes[i].ValidatorIndex) < uint64(doubleVotes[j].ValidatorIndex)
+			})
+			require.Equal(t, len(wanted), len(doubleVotes))
+			for i, double := range doubleVotes {
+				require.DeepEqual(t, wanted[i].ValidatorIndex, double.ValidatorIndex)
+				require.DeepEqual(t, wanted[i].Target, double.Target)
+				require.DeepEqual(t, wanted[i].Wrapper_1, double.Wrapper_1)
+				require.DeepEqual(t, wanted[i].Wrapper_2, double.Wrapper_2)
+			}
+		})
 	}
 }

@@ -376,12 +415,20 @@ func Test_encodeDecodeAttestationRecord(t *testing.T) {
 		wantErr    bool
 	}{
 		{
-			name:       "empty standard encode/decode",
-			attWrapper: createAttestationWrapper(0, 0, nil /* indices */, nil /* signingRoot */),
+			name:       "phase0 empty standard encode/decode",
+			attWrapper: createAttestationWrapper(version.Phase0, 0, 0, nil /* indices */, nil /* signingRoot */),
 		},
 		{
-			name:       "standard encode/decode",
-			attWrapper: createAttestationWrapper(15, 6, []uint64{2, 4}, []byte("1") /* signingRoot */),
+			name:       "phase0 standard encode/decode",
+			attWrapper: createAttestationWrapper(version.Phase0, 15, 6, []uint64{2, 4}, []byte("1") /* signingRoot */),
+		},
+		{
+			name:       "electra empty standard encode/decode",
+			attWrapper: createAttestationWrapper(version.Electra, 0, 0, nil /* indices */, nil /* signingRoot */),
+		},
+		{
+			name:       "electra standard encode/decode",
+			attWrapper: createAttestationWrapper(version.Electra, 15, 6, []uint64{2, 4}, []byte("1") /* signingRoot */),
 		},
 		{
 			name: "failing encode/decode",
@@ -433,7 +480,7 @@ func TestStore_HighestAttestations(t *testing.T) {
 		{
 			name: "should get highest att if single att in db",
 			attestationsInDB: []*slashertypes.IndexedAttestationWrapper{
-				createAttestationWrapper(0, 3, []uint64{1}, []byte{1}),
+				createAttestationWrapper(version.Phase0, 0, 3, []uint64{1}, []byte{1}),
 			},
 			indices: []primitives.ValidatorIndex{1},
 			expected: []*ethpb.HighestAttestation{
@@ -447,10 +494,10 @@ func TestStore_HighestAttestations(t *testing.T) {
 		{
 			name: "should get highest att for multiple with diff histories",
 			attestationsInDB: []*slashertypes.IndexedAttestationWrapper{
-				createAttestationWrapper(0, 3, []uint64{2}, []byte{1}),
-				createAttestationWrapper(1, 4, []uint64{3}, []byte{2}),
-				createAttestationWrapper(2, 3, []uint64{4}, []byte{3}),
-				createAttestationWrapper(5, 6, []uint64{5}, []byte{4}),
+				createAttestationWrapper(version.Phase0, 0, 3, []uint64{2}, []byte{1}),
+				createAttestationWrapper(version.Phase0, 1, 4, []uint64{3}, []byte{2}),
+				createAttestationWrapper(version.Phase0, 2, 3, []uint64{4}, []byte{3}),
+				createAttestationWrapper(version.Phase0, 5, 6, []uint64{5}, []byte{4}),
 			},
 			indices: []primitives.ValidatorIndex{2, 3, 4, 5},
 			expected: []*ethpb.HighestAttestation{
@@ -479,10 +526,10 @@ func TestStore_HighestAttestations(t *testing.T) {
 		{
 			name: "should get correct highest att for multiple shared atts with diff histories",
 			attestationsInDB: []*slashertypes.IndexedAttestationWrapper{
-				createAttestationWrapper(1, 4, []uint64{2, 3}, []byte{1}),
-				createAttestationWrapper(2, 5, []uint64{3, 5}, []byte{2}),
-				createAttestationWrapper(4, 5, []uint64{1, 2}, []byte{3}),
-				createAttestationWrapper(6, 7, []uint64{5}, []byte{4}),
+				createAttestationWrapper(version.Phase0, 1, 4, []uint64{2, 3}, []byte{1}),
+				createAttestationWrapper(version.Phase0, 2, 5, []uint64{3, 5}, []byte{2}),
+				createAttestationWrapper(version.Phase0, 4, 5, []uint64{1, 2}, []byte{3}),
+				createAttestationWrapper(version.Phase0, 6, 7, []uint64{5}, []byte{4}),
 			},
 			indices: []primitives.ValidatorIndex{2, 3, 4, 5},
 			expected: []*ethpb.HighestAttestation{
@@ -533,7 +580,7 @@ func BenchmarkHighestAttestations(b *testing.B) {
 	}
 	atts := make([]*slashertypes.IndexedAttestationWrapper, count)
 	for i := 0; i < count; i++ {
-		atts[i] = createAttestationWrapper(primitives.Epoch(i), primitives.Epoch(i+2), indicesPerAtt[i], []byte{})
+		atts[i] = createAttestationWrapper(version.Phase0, primitives.Epoch(i), primitives.Epoch(i+2), indicesPerAtt[i], []byte{})
 	}

 	ctx := context.Background()
@@ -570,7 +617,7 @@ func BenchmarkStore_CheckDoubleBlockProposals(b *testing.B) {
 	}
 	atts := make([]*slashertypes.IndexedAttestationWrapper, count)
 	for i := 0; i < count; i++ {
-		atts[i] = createAttestationWrapper(primitives.Epoch(i), primitives.Epoch(i+2), indicesPerAtt[i], []byte{})
+		atts[i] = createAttestationWrapper(version.Phase0, primitives.Epoch(i), primitives.Epoch(i+2), indicesPerAtt[i], []byte{})
 	}

 	ctx := context.Background()
@@ -609,7 +656,7 @@ func createProposalWrapper(t *testing.T, slot primitives.Slot, proposerIndex pri
 	}
 }

-func createAttestationWrapper(source, target primitives.Epoch, indices []uint64, dataRootBytes []byte) *slashertypes.IndexedAttestationWrapper {
+func createAttestationWrapper(ver int, source, target primitives.Epoch, indices []uint64, dataRootBytes []byte) *slashertypes.IndexedAttestationWrapper {
 	dataRoot := bytesutil.ToBytes32(dataRootBytes)
 	if dataRootBytes == nil {
 		dataRoot = params.BeaconConfig().ZeroHash
@@ -627,6 +674,16 @@ func createAttestationWrapper(source, target primitives.Epoch, indices []uint64,
 		},
 	}

+	if ver >= version.Electra {
+		return &slashertypes.IndexedAttestationWrapper{
+			IndexedAttestation: &ethpb.IndexedAttestationElectra{
+				AttestingIndices: indices,
+				Data:             data,
+				Signature:        params.BeaconConfig().EmptySignature[:],
+			},
+			DataRoot: dataRoot,
+		}
+	}
 	return &slashertypes.IndexedAttestationWrapper{
 		IndexedAttestation: &ethpb.IndexedAttestation{
 			AttestingIndices: indices,
--- a/beacon-chain/db/slasherkv/slasherkv_test.go
+++ b/beacon-chain/db/slasherkv/slasherkv_test.go
@@ -2,6 +2,7 @@ package slasherkv

 import (
 	"io"
+	"os"
 	"testing"

 	"github.com/sirupsen/logrus"
@@ -10,5 +11,5 @@ import (
 func TestMain(m *testing.M) {
 	logrus.SetLevel(logrus.DebugLevel)
 	logrus.SetOutput(io.Discard)
-	m.Run()
+	os.Exit(m.Run())
 }
--- a/beacon-chain/execution/BUILD.bazel
+++ b/beacon-chain/execution/BUILD.bazel
@@ -103,6 +103,7 @@ go_test(
        "//beacon-chain/core/helpers:go_default_library",
        "//beacon-chain/core/signing:go_default_library",
        "//beacon-chain/db:go_default_library",
+        "//beacon-chain/db/filesystem:go_default_library",
        "//beacon-chain/db/testing:go_default_library",
        "//beacon-chain/execution/testing:go_default_library",
        "//beacon-chain/execution/types:go_default_library",
--- a/beacon-chain/execution/engine_client.go
+++ b/beacon-chain/execution/engine_client.go
@@ -105,7 +105,7 @@ type Reconstructor interface {
 	ReconstructFullBellatrixBlockBatch(
 		ctx context.Context, blindedBlocks []interfaces.ReadOnlySignedBeaconBlock,
 	) ([]interfaces.SignedBeaconBlock, error)
-	ReconstructBlobSidecars(ctx context.Context, block interfaces.ReadOnlySignedBeaconBlock, blockRoot [32]byte, indices []bool) ([]blocks.VerifiedROBlob, error)
+	ReconstructBlobSidecars(ctx context.Context, block interfaces.ReadOnlySignedBeaconBlock, blockRoot [32]byte, hi func(uint64) bool) ([]blocks.VerifiedROBlob, error)
 }

 // EngineCaller defines a client that can interact with an Ethereum
@@ -531,32 +531,23 @@ func (s *Service) ReconstructFullBellatrixBlockBatch(
 // It retrieves the KZG commitments from the block body, fetches the associated blobs and proofs,
 // and constructs the corresponding verified read-only blob sidecars.
 //
-// The 'exists' argument is a boolean list (must be the same length as body.BlobKzgCommitments), where each element corresponds to whether a
-// particular blob sidecar already exists. If exists[i] is true, the blob for the i-th KZG commitment
-// has already been retrieved and does not need to be fetched again from the execution layer (EL).
-//
-// For example:
-//   - len(block.Body().BlobKzgCommitments()) == 6
-//   - If exists = [true, false, true, false, true, false], the function will fetch the blobs
-//     associated with indices 1, 3, and 5 (since those are marked as non-existent).
-//   - If exists = [false ... x 6], the function will attempt to fetch all blobs.
-//
-// Only the blobs that do not already exist (where exists[i] is false) are fetched using the KZG commitments from block body.
-func (s *Service) ReconstructBlobSidecars(ctx context.Context, block interfaces.ReadOnlySignedBeaconBlock, blockRoot [32]byte, exists []bool) ([]blocks.VerifiedROBlob, error) {
+// The 'hasIndex' argument is a function returns true if the given uint64 blob index already exists on disc.
+// Only the blobs that do not already exist (where hasIndex(i) is false)
+// will be fetched from the execution engine using the KZG commitments from block body.
+func (s *Service) ReconstructBlobSidecars(ctx context.Context, block interfaces.ReadOnlySignedBeaconBlock, blockRoot [32]byte, hasIndex func(uint64) bool) ([]blocks.VerifiedROBlob, error) {
 	blockBody := block.Block().Body()
 	kzgCommitments, err := blockBody.BlobKzgCommitments()
 	if err != nil {
 		return nil, errors.Wrap(err, "could not get blob KZG commitments")
 	}
-	if len(kzgCommitments) > len(exists) {
-		return nil, fmt.Errorf("length of KZG commitments (%d) is greater than length of exists (%d)", len(kzgCommitments), len(exists))
-	}

 	// Collect KZG hashes for non-existing blobs
 	var kzgHashes []common.Hash
+	var kzgIndexes []int
 	for i, commitment := range kzgCommitments {
-		if !exists[i] {
+		if !hasIndex(uint64(i)) {
 			kzgHashes = append(kzgHashes, primitives.ConvertKzgCommitmentToVersionedHash(commitment))
+			kzgIndexes = append(kzgIndexes, i)
 		}
 	}
 	if len(kzgHashes) == 0 {
@@ -579,27 +570,21 @@ func (s *Service) ReconstructBlobSidecars(ctx context.Context, block interfaces.

 	// Reconstruct verified blob sidecars
 	var verifiedBlobs []blocks.VerifiedROBlob
-	for i, blobIndex := 0, 0; i < len(kzgCommitments); i++ {
-		if exists[i] {
+	for i := 0; i < len(kzgHashes); i++ {
+		if blobs[i] == nil {
 			continue
 		}
-
-		if blobIndex >= len(blobs) || blobs[blobIndex] == nil {
-			blobIndex++
-			continue
-		}
-		blob := blobs[blobIndex]
-		blobIndex++
-
-		proof, err := blocks.MerkleProofKZGCommitment(blockBody, i)
+		blob := blobs[i]
+		blobIndex := kzgIndexes[i]
+		proof, err := blocks.MerkleProofKZGCommitment(blockBody, blobIndex)
 		if err != nil {
-			log.WithError(err).WithField("index", i).Error("failed to get Merkle proof for KZG commitment")
+			log.WithError(err).WithField("index", blobIndex).Error("failed to get Merkle proof for KZG commitment")
 			continue
 		}
 		sidecar := &ethpb.BlobSidecar{
-			Index:                    uint64(i),
+			Index:                    uint64(blobIndex),
 			Blob:                     blob.Blob,
-			KzgCommitment:            kzgCommitments[i],
+			KzgCommitment:            kzgCommitments[blobIndex],
 			KzgProof:                 blob.KzgProof,
 			SignedBlockHeader:        header,
 			CommitmentInclusionProof: proof,
@@ -607,14 +592,14 @@ func (s *Service) ReconstructBlobSidecars(ctx context.Context, block interfaces.

 		roBlob, err := blocks.NewROBlobWithRoot(sidecar, blockRoot)
 		if err != nil {
-			log.WithError(err).WithField("index", i).Error("failed to create RO blob with root")
+			log.WithError(err).WithField("index", blobIndex).Error("failed to create RO blob with root")
 			continue
 		}

 		v := s.blobVerifier(roBlob, verification.ELMemPoolRequirements)
 		verifiedBlob, err := v.VerifiedROBlob()
 		if err != nil {
-			log.WithError(err).WithField("index", i).Error("failed to verify RO blob")
+			log.WithError(err).WithField("index", blobIndex).Error("failed to verify RO blob")
 			continue
 		}

--- a/beacon-chain/execution/engine_client_test.go
+++ b/beacon-chain/execution/engine_client_test.go
@@ -20,6 +20,7 @@ import (
 	"github.com/ethereum/go-ethereum/rpc"
 	"github.com/holiman/uint256"
 	"github.com/pkg/errors"
+	"github.com/prysmaticlabs/prysm/v5/beacon-chain/db/filesystem"
 	mocks "github.com/prysmaticlabs/prysm/v5/beacon-chain/execution/testing"
 	"github.com/prysmaticlabs/prysm/v5/beacon-chain/verification"
 	fieldparams "github.com/prysmaticlabs/prysm/v5/config/fieldparams"
@@ -2395,6 +2396,12 @@ func Test_ExchangeCapabilities(t *testing.T) {
 	})
 }

+func mockSummary(t *testing.T, exists []bool) func(uint64) bool {
+	hi, err := filesystem.NewBlobStorageSummary(params.BeaconConfig().DenebForkEpoch, exists)
+	require.NoError(t, err)
+	return hi.HasIndex
+}
+
 func TestReconstructBlobSidecars(t *testing.T) {
 	client := &Service{capabilityCache: &capabilityCache{}}
 	b := util.NewBeaconBlockDeneb()
@@ -2408,15 +2415,15 @@ func TestReconstructBlobSidecars(t *testing.T) {

 	ctx := context.Background()
 	t.Run("all seen", func(t *testing.T) {
-		exists := []bool{true, true, true, true, true, true}
-		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, exists)
+		hi := mockSummary(t, []bool{true, true, true, true, true, true})
+		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, hi)
 		require.NoError(t, err)
 		require.Equal(t, 0, len(verifiedBlobs))
 	})

 	t.Run("get-blobs end point is not supported", func(t *testing.T) {
-		exists := []bool{true, true, true, true, true, false}
-		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, exists)
+		hi := mockSummary(t, []bool{true, true, true, true, true, false})
+		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, hi)
 		require.NoError(t, err)
 		require.Equal(t, 0, len(verifiedBlobs))
 	})
@@ -2430,8 +2437,8 @@ func TestReconstructBlobSidecars(t *testing.T) {
 		rpcClient, client := setupRpcClient(t, srv.URL, client)
 		defer rpcClient.Close()

-		exists := [6]bool{}
-		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, exists[:])
+		hi := mockSummary(t, make([]bool, 6))
+		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, hi)
 		require.NoError(t, err)
 		require.Equal(t, 6, len(verifiedBlobs))
 	})
@@ -2443,22 +2450,29 @@ func TestReconstructBlobSidecars(t *testing.T) {
 		rpcClient, client := setupRpcClient(t, srv.URL, client)
 		defer rpcClient.Close()

-		exists := []bool{true, false, true, false, true, false}
-		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, exists)
+		hi := mockSummary(t, []bool{true, false, true, false, true, false})
+		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, hi)
 		require.NoError(t, err)
 		require.Equal(t, 3, len(verifiedBlobs))
 	})

-	t.Run("kzg is longer than exist", func(t *testing.T) {
-		srv := createBlobServer(t, 3)
+	t.Run("recovered 3 missing blobs with mutated blob mask", func(t *testing.T) {
+		exists := []bool{true, false, true, false, true, false}
+		hi := mockSummary(t, exists)
+
+		srv := createBlobServer(t, 3, func() {
+			// Mutate blob mask
+			exists[1] = true
+			exists[3] = true
+		})
 		defer srv.Close()

 		rpcClient, client := setupRpcClient(t, srv.URL, client)
 		defer rpcClient.Close()

-		exists := []bool{true, false, true, false, true}
-		_, err := client.ReconstructBlobSidecars(ctx, sb, r, exists)
-		require.ErrorContains(t, "length of KZG commitments (6) is greater than length of exists (5)", err)
+		verifiedBlobs, err := client.ReconstructBlobSidecars(ctx, sb, r, hi)
+		require.NoError(t, err)
+		require.Equal(t, 3, len(verifiedBlobs))
 	})
 }

@@ -2472,12 +2486,16 @@ func createRandomKzgCommitments(t *testing.T, num int) [][]byte {
 	return kzgCommitments
 }

-func createBlobServer(t *testing.T, numBlobs int) *httptest.Server {
+func createBlobServer(t *testing.T, numBlobs int, callbackFuncs ...func()) *httptest.Server {
 	return httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 		w.Header().Set("Content-Type", "application/json")
 		defer func() {
 			require.NoError(t, r.Body.Close())
 		}()
+		// Execute callback functions for each request.
+		for _, f := range callbackFuncs {
+			f()
+		}

 		blobs := make([]pb.BlobAndProofJson, numBlobs)
 		for i := range blobs {
--- a/beacon-chain/execution/execution_chain_test.go
+++ b/beacon-chain/execution/execution_chain_test.go
@@ -2,6 +2,7 @@ package execution

 import (
 	"io"
+	"os"
 	"testing"

 	"github.com/sirupsen/logrus"
@@ -11,5 +12,5 @@ func TestMain(m *testing.M) {
 	logrus.SetLevel(logrus.DebugLevel)
 	logrus.SetOutput(io.Discard)

-	m.Run()
+	os.Exit(m.Run())
 }
--- a/beacon-chain/execution/testing/mock_engine_client.go
+++ b/beacon-chain/execution/testing/mock_engine_client.go
@@ -109,7 +109,7 @@ func (e *EngineClient) ReconstructFullBellatrixBlockBatch(
 }

 // ReconstructBlobSidecars is a mock implementation of the ReconstructBlobSidecars method.
-func (e *EngineClient) ReconstructBlobSidecars(context.Context, interfaces.ReadOnlySignedBeaconBlock, [32]byte, []bool) ([]blocks.VerifiedROBlob, error) {
+func (e *EngineClient) ReconstructBlobSidecars(context.Context, interfaces.ReadOnlySignedBeaconBlock, [32]byte, func(uint64) bool) ([]blocks.VerifiedROBlob, error) {
 	return e.BlobSidecars, e.ErrorBlobSidecars
 }

--- a/beacon-chain/forkchoice/doubly-linked-tree/reorg_late_blocks.go
+++ b/beacon-chain/forkchoice/doubly-linked-tree/reorg_late_blocks.go
@@ -78,7 +78,7 @@ func (f *ForkChoice) ShouldOverrideFCU() (override bool) {
 	// }

 	// Only orphan a block if the head LMD vote is weak
-	if head.weight*100 > f.store.committeeWeight*params.BeaconConfig().ReorgWeightThreshold {
+	if head.weight*100 > f.store.committeeWeight*params.BeaconConfig().ReorgHeadWeightThreshold {
 		return
 	}

@@ -143,7 +143,7 @@ func (f *ForkChoice) GetProposerHead() [32]byte {
 	}

 	// Only orphan a block if the head LMD vote is weak
-	if head.weight*100 > f.store.committeeWeight*params.BeaconConfig().ReorgWeightThreshold {
+	if head.weight*100 > f.store.committeeWeight*params.BeaconConfig().ReorgHeadWeightThreshold {
 		return head.root
 	}

--- a/Show More
+++ b/Show More
@@ -1 +1 @@
 .1.0
 .4.1