diff --git a/crates/engine/tree/src/tree/payload_processor/mod.rs b/crates/engine/tree/src/tree/payload_processor/mod.rs
index 8558a7479e..af9a2548ce 100644
--- a/crates/engine/tree/src/tree/payload_processor/mod.rs
+++ b/crates/engine/tree/src/tree/payload_processor/mod.rs
@@ -31,6 +31,7 @@ use reth_trie_parallel::{
 use std::{
     collections::VecDeque,
     sync::{
+        atomic::AtomicBool,
         mpsc,
         mpsc::{channel, Sender},
         Arc,
@@ -251,6 +252,7 @@ where
             cache_metrics: cache_metrics.clone(),
             provider: provider_builder,
             metrics: PrewarmMetrics::default(),
+            terminate_execution: Arc::new(AtomicBool::new(false)),
         };
 
         let prewarm_task = PrewarmCacheTask::new(
diff --git a/crates/engine/tree/src/tree/payload_processor/prewarm.rs b/crates/engine/tree/src/tree/payload_processor/prewarm.rs
index 07502141a0..4d94f7b84c 100644
--- a/crates/engine/tree/src/tree/payload_processor/prewarm.rs
+++ b/crates/engine/tree/src/tree/payload_processor/prewarm.rs
@@ -20,7 +20,11 @@ use reth_revm::{database::StateProviderDatabase, db::BundleState, state::EvmStat
 use reth_trie::MultiProofTargets;
 use std::{
     collections::VecDeque,
-    sync::mpsc::{channel, Receiver, Sender},
+    sync::{
+        atomic::{AtomicBool, Ordering},
+        mpsc::{channel, Receiver, Sender},
+        Arc,
+    },
     time::Instant,
 };
 use tracing::{debug, trace};
@@ -46,6 +50,8 @@ pub(super) struct PrewarmCacheTask<N: NodePrimitives, P, Evm> {
     actions_rx: Receiver<PrewarmTaskEvent>,
     /// Sender the transactions use to send their result back
     actions_tx: Sender<PrewarmTaskEvent>,
+    /// Total prewarming tasks spawned
+    prewarm_outcomes_left: usize,
 }
 
 impl<N, P, Evm> PrewarmCacheTask<N, P, Evm>
@@ -72,6 +78,7 @@ where
             to_multi_proof,
             actions_rx,
             actions_tx,
+            prewarm_outcomes_left: 0,
         }
     }
 
@@ -89,6 +96,7 @@ where
             let ctx = self.ctx.clone();
             let pending_chunk = chunk.collect::<Vec<_>>();
 
+            self.prewarm_outcomes_left += pending_chunk.len();
             self.executor.spawn_blocking(move || {
                 ctx.transact_batch(&pending_chunk, sender);
             });
@@ -103,7 +111,7 @@ where
     }
 
     /// Save the state to the shared cache for the given block.
-    fn save_cache(&self, state: BundleState) {
+    fn save_cache(self, state: BundleState) {
         let start = Instant::now();
         let cache = SavedCache::new(
             self.ctx.header.hash(),
@@ -123,6 +131,15 @@ where
         self.ctx.metrics.cache_saving_duration.set(start.elapsed().as_secs_f64());
     }
 
+    /// Removes the `actions_tx` currently stored in the struct, replacing it with a new one that
+    /// does not point to any active receiver.
+    ///
+    /// This is used to drop the `actions_tx` after all tasks have been spawned, and should not be
+    /// used in any context other than the `run` method.
+    fn drop_actions_tx(&mut self) {
+        self.actions_tx = channel().0;
+    }
+
     /// Executes the task.
     ///
     /// This will execute the transactions until all transactions have been processed or the task
@@ -134,26 +151,45 @@ where
         // spawn execution tasks.
         self.spawn_all();
 
+        // drop the actions sender after we've spawned all execution tasks. This is so that the
+        // following loop can terminate even if one of the prewarm tasks ends in an error (i.e.,
+        // does not return an Outcome) or panics.
+        self.drop_actions_tx();
+
+        let mut final_block_output = None;
         while let Ok(event) = self.actions_rx.recv() {
             match event {
                 PrewarmTaskEvent::TerminateTransactionExecution => {
                     // stop tx processing
-                    self.pending.clear();
+                    self.ctx.terminate_execution.store(true, Ordering::Relaxed);
                 }
                 PrewarmTaskEvent::Outcome { proof_targets } => {
-                    // completed a transaction, frees up one slot
+                    // completed executing a set of transactions
                     self.send_multi_proof_targets(proof_targets);
+
+                    // decrement the number of tasks left
+                    self.prewarm_outcomes_left -= 1;
+
+                    if self.prewarm_outcomes_left == 0 && final_block_output.is_some() {
+                        // all tasks are done, and we have the block output, we can exit
+                        break
+                    }
                 }
                 PrewarmTaskEvent::Terminate { block_output } => {
-                    // terminate the task
-                    if let Some(state) = block_output {
-                        self.save_cache(state);
-                    }
+                    final_block_output = Some(block_output);
 
-                    break
+                    if self.prewarm_outcomes_left == 0 {
+                        // all tasks are done, we can exit, which will save caches and exit
+                        break
+                    }
                 }
             }
         }
+
+        // save caches and finish
+        if let Some(Some(state)) = final_block_output {
+            self.save_cache(state);
+        }
     }
 }
 
@@ -167,6 +203,8 @@ pub(super) struct PrewarmContext<N: NodePrimitives, P, Evm> {
     /// Provider to obtain the state
     pub(super) provider: StateProviderBuilder<N, P>,
     pub(super) metrics: PrewarmMetrics,
+    /// An atomic bool that tells prewarm tasks to not start any more execution.
+    pub(super) terminate_execution: Arc<AtomicBool>,
 }
 
 impl<N, P, Evm> PrewarmContext<N, P, Evm>
@@ -175,9 +213,20 @@ where
     P: BlockReader + StateProviderFactory + StateReader + StateCommitmentProvider + Clone + 'static,
     Evm: ConfigureEvm<Primitives = N> + 'static,
 {
-    /// Splits this context into an evm, an evm config, and metrics.
-    fn evm_for_ctx(self) -> Option<(EvmFor<Evm, impl Database>, Evm, PrewarmMetrics)> {
-        let Self { header, evm_config, cache: caches, cache_metrics, provider, metrics } = self;
+    /// Splits this context into an evm, an evm config, metrics, and the atomic bool for terminating
+    /// execution.
+    fn evm_for_ctx(
+        self,
+    ) -> Option<(EvmFor<Evm, impl Database>, Evm, PrewarmMetrics, Arc<AtomicBool>)> {
+        let Self {
+            header,
+            evm_config,
+            cache: caches,
+            cache_metrics,
+            provider,
+            metrics,
+            terminate_execution,
+        } = self;
 
         let state_provider = match provider.build() {
             Ok(provider) => provider,
@@ -206,7 +255,7 @@ where
         // create a new executor and disable nonce checks in the env
         let evm = evm_config.evm_with_env(state_provider, evm_env);
 
-        Some((evm, evm_config, metrics))
+        Some((evm, evm_config, metrics, terminate_execution))
     }
 
     /// Transacts the vec of transactions and returns the state outcome.
@@ -217,9 +266,18 @@ where
     /// Note: Since here are no ordering guarantees this won't the state the txs produce when
     /// executed sequentially.
     fn transact_batch(self, txs: &[Recovered<N::SignedTx>], sender: Sender<PrewarmTaskEvent>) {
-        let Some((mut evm, evm_config, metrics)) = self.evm_for_ctx() else { return };
+        let Some((mut evm, evm_config, metrics, terminate_execution)) = self.evm_for_ctx() else {
+            return
+        };
 
         for tx in txs {
+            // If the task was cancelled, stop execution, send an empty result to notify the task,
+            // and exit.
+            if terminate_execution.load(Ordering::Relaxed) {
+                let _ = sender.send(PrewarmTaskEvent::Outcome { proof_targets: None });
+                return
+            }
+
             // create the tx env
             let tx_env = evm_config.tx_env(tx);
             let start = Instant::now();