diff --git a/src/cli/gateway-cli/run-loop.ts b/src/cli/gateway-cli/run-loop.ts
index 9cdcf18652..9486e199e3 100644
--- a/src/cli/gateway-cli/run-loop.ts
+++ b/src/cli/gateway-cli/run-loop.ts
@@ -6,6 +6,7 @@ import {
   isGatewaySigusr1RestartExternallyAllowed,
 } from "../../infra/restart.js";
 import { createSubsystemLogger } from "../../logging/subsystem.js";
+import { getActiveTaskCount, waitForActiveTasks } from "../../process/command-queue.js";
 
 const gatewayLog = createSubsystemLogger("gateway");
 
@@ -26,6 +27,9 @@ export async function runGatewayLoop(params: {
     process.removeListener("SIGUSR1", onSigusr1);
   };
 
+  const DRAIN_TIMEOUT_MS = 30_000;
+  const SHUTDOWN_TIMEOUT_MS = 5_000;
+
   const request = (action: GatewayRunSignalAction, signal: string) => {
     if (shuttingDown) {
       gatewayLog.info(`received ${signal} during shutdown; ignoring`);
@@ -35,14 +39,33 @@ export async function runGatewayLoop(params: {
     const isRestart = action === "restart";
     gatewayLog.info(`received ${signal}; ${isRestart ? "restarting" : "shutting down"}`);
 
+    // Allow extra time for draining active turns on restart.
+    const forceExitMs = isRestart ? DRAIN_TIMEOUT_MS + SHUTDOWN_TIMEOUT_MS : SHUTDOWN_TIMEOUT_MS;
     const forceExitTimer = setTimeout(() => {
       gatewayLog.error("shutdown timed out; exiting without full cleanup");
       cleanupSignals();
       params.runtime.exit(0);
-    }, 5000);
+    }, forceExitMs);
 
     void (async () => {
       try {
+        // On restart, wait for in-flight agent turns to finish before
+        // tearing down the server so buffered messages are delivered.
+        if (isRestart) {
+          const activeTasks = getActiveTaskCount();
+          if (activeTasks > 0) {
+            gatewayLog.info(
+              `draining ${activeTasks} active task(s) before restart (timeout ${DRAIN_TIMEOUT_MS}ms)`,
+            );
+            const { drained } = await waitForActiveTasks(DRAIN_TIMEOUT_MS);
+            if (drained) {
+              gatewayLog.info("all active tasks drained");
+            } else {
+              gatewayLog.warn("drain timeout reached; proceeding with restart");
+            }
+          }
+        }
+
         await server?.close({
           reason: isRestart ? "gateway restarting" : "gateway stopping",
           restartExpectedMs: isRestart ? 1500 : null,
diff --git a/src/process/command-queue.test.ts b/src/process/command-queue.test.ts
index 8ede381da9..d08688347c 100644
--- a/src/process/command-queue.test.ts
+++ b/src/process/command-queue.test.ts
@@ -16,7 +16,14 @@ vi.mock("../logging/diagnostic.js", () => ({
   diagnosticLogger: diagnosticMocks.diag,
 }));
 
-import { enqueueCommand, getQueueSize } from "./command-queue.js";
+import {
+  enqueueCommand,
+  enqueueCommandInLane,
+  getActiveTaskCount,
+  getQueueSize,
+  setCommandLaneConcurrency,
+  waitForActiveTasks,
+} from "./command-queue.js";
 
 describe("command queue", () => {
   beforeEach(() => {
@@ -85,4 +92,106 @@ describe("command queue", () => {
     expect(waited as number).toBeGreaterThanOrEqual(5);
     expect(queuedAhead).toBe(0);
   });
+
+  it("getActiveTaskCount returns count of currently executing tasks", async () => {
+    let resolve1!: () => void;
+    const blocker = new Promise<void>((r) => {
+      resolve1 = r;
+    });
+
+    const task = enqueueCommand(async () => {
+      await blocker;
+    });
+
+    // Give the event loop a tick for the task to start.
+    await new Promise((r) => setTimeout(r, 5));
+    expect(getActiveTaskCount()).toBe(1);
+
+    resolve1();
+    await task;
+    expect(getActiveTaskCount()).toBe(0);
+  });
+
+  it("waitForActiveTasks resolves immediately when no tasks are active", async () => {
+    const { drained } = await waitForActiveTasks(1000);
+    expect(drained).toBe(true);
+  });
+
+  it("waitForActiveTasks waits for active tasks to finish", async () => {
+    let resolve1!: () => void;
+    const blocker = new Promise<void>((r) => {
+      resolve1 = r;
+    });
+
+    const task = enqueueCommand(async () => {
+      await blocker;
+    });
+
+    // Give the task a tick to start.
+    await new Promise((r) => setTimeout(r, 5));
+
+    const drainPromise = waitForActiveTasks(5000);
+
+    // Resolve the blocker after a short delay.
+    setTimeout(() => resolve1(), 50);
+
+    const { drained } = await drainPromise;
+    expect(drained).toBe(true);
+
+    await task;
+  });
+
+  it("waitForActiveTasks returns drained=false on timeout", async () => {
+    let resolve1!: () => void;
+    const blocker = new Promise<void>((r) => {
+      resolve1 = r;
+    });
+
+    const task = enqueueCommand(async () => {
+      await blocker;
+    });
+
+    await new Promise((r) => setTimeout(r, 5));
+
+    const { drained } = await waitForActiveTasks(50);
+    expect(drained).toBe(false);
+
+    resolve1();
+    await task;
+  });
+
+  it("waitForActiveTasks ignores tasks that start after the call", async () => {
+    const lane = `drain-snapshot-${Date.now()}-${Math.random().toString(16).slice(2)}`;
+    setCommandLaneConcurrency(lane, 2);
+
+    let resolve1!: () => void;
+    const blocker1 = new Promise<void>((r) => {
+      resolve1 = r;
+    });
+    let resolve2!: () => void;
+    const blocker2 = new Promise<void>((r) => {
+      resolve2 = r;
+    });
+
+    const first = enqueueCommandInLane(lane, async () => {
+      await blocker1;
+    });
+    await new Promise((r) => setTimeout(r, 5));
+
+    const drainPromise = waitForActiveTasks(2000);
+
+    // Starts after waitForActiveTasks snapshot and should not block drain completion.
+    const second = enqueueCommandInLane(lane, async () => {
+      await blocker2;
+    });
+    await new Promise((r) => setTimeout(r, 5));
+    expect(getActiveTaskCount()).toBeGreaterThanOrEqual(2);
+
+    resolve1();
+    const { drained } = await drainPromise;
+    expect(drained).toBe(true);
+
+    resolve2();
+    await Promise.all([first, second]);
+  });
 });
diff --git a/src/process/command-queue.ts b/src/process/command-queue.ts
index f9f2f0093f..205cb16013 100644
--- a/src/process/command-queue.ts
+++ b/src/process/command-queue.ts
@@ -19,11 +19,13 @@ type LaneState = {
   lane: string;
   queue: QueueEntry[];
   active: number;
+  activeTaskIds: Set<number>;
   maxConcurrent: number;
   draining: boolean;
 };
 
 const lanes = new Map<string, LaneState>();
+let nextTaskId = 1;
 
 function getLaneState(lane: string): LaneState {
   const existing = lanes.get(lane);
@@ -34,6 +36,7 @@ function getLaneState(lane: string): LaneState {
     lane,
     queue: [],
     active: 0,
+    activeTaskIds: new Set(),
     maxConcurrent: 1,
     draining: false,
   };
@@ -59,12 +62,15 @@ function drainLane(lane: string) {
         );
       }
       logLaneDequeue(lane, waitedMs, state.queue.length);
+      const taskId = nextTaskId++;
       state.active += 1;
+      state.activeTaskIds.add(taskId);
       void (async () => {
         const startTime = Date.now();
         try {
           const result = await entry.task();
           state.active -= 1;
+          state.activeTaskIds.delete(taskId);
           diag.debug(
             `lane task done: lane=${lane} durationMs=${Date.now() - startTime} active=${state.active} queued=${state.queue.length}`,
           );
@@ -72,6 +78,7 @@ function drainLane(lane: string) {
           entry.resolve(result);
         } catch (err) {
           state.active -= 1;
+          state.activeTaskIds.delete(taskId);
           const isProbeLane = lane.startsWith("auth-probe:") || lane.startsWith("session:probe-");
           if (!isProbeLane) {
             diag.error(
@@ -158,3 +165,67 @@ export function clearCommandLane(lane: string = CommandLane.Main) {
   state.queue.length = 0;
   return removed;
 }
+
+/**
+ * Returns the total number of actively executing tasks across all lanes
+ * (excludes queued-but-not-started entries).
+ */
+export function getActiveTaskCount(): number {
+  let total = 0;
+  for (const s of lanes.values()) {
+    total += s.active;
+  }
+  return total;
+}
+
+/**
+ * Wait for all currently active tasks across all lanes to finish.
+ * Polls at a short interval; resolves when no tasks are active or
+ * when `timeoutMs` elapses (whichever comes first).
+ *
+ * New tasks enqueued after this call are ignored — only tasks that are
+ * already executing are waited on.
+ */
+export function waitForActiveTasks(timeoutMs: number): Promise<{ drained: boolean }> {
+  const POLL_INTERVAL_MS = 250;
+  const deadline = Date.now() + timeoutMs;
+  const activeAtStart = new Set<number>();
+  for (const state of lanes.values()) {
+    for (const taskId of state.activeTaskIds) {
+      activeAtStart.add(taskId);
+    }
+  }
+
+  return new Promise((resolve) => {
+    const check = () => {
+      if (activeAtStart.size === 0) {
+        resolve({ drained: true });
+        return;
+      }
+
+      let hasPending = false;
+      for (const state of lanes.values()) {
+        for (const taskId of state.activeTaskIds) {
+          if (activeAtStart.has(taskId)) {
+            hasPending = true;
+            break;
+          }
+        }
+        if (hasPending) {
+          break;
+        }
+      }
+
+      if (!hasPending) {
+        resolve({ drained: true });
+        return;
+      }
+      if (Date.now() >= deadline) {
+        resolve({ drained: false });
+        return;
+      }
+      setTimeout(check, POLL_INTERVAL_MS);
+    };
+    check();
+  });
+}