diff --git a/.changeset/guard-agent-task-handoff-run-state.md b/.changeset/guard-agent-task-handoff-run-state.md
new file mode 100644
index 000000000..6a737d9db
--- /dev/null
+++ b/.changeset/guard-agent-task-handoff-run-state.md
@@ -0,0 +1,5 @@
+---
+'@livekit/agents': patch
+---
+
+Fix `session.run()` stalling or racing the activity transition when an AgentTask handoff is triggered by a speech that predates the run (e.g. created in `onEnter`): the blocked handoff tasks are now watched by the active run for the duration of the transition.
diff --git a/agents/src/voice/agent.ts b/agents/src/voice/agent.ts
index 47a2a3dd4..05536663b 100644
--- a/agents/src/voice/agent.ts
+++ b/agents/src/voice/agent.ts
@@ -684,6 +684,13 @@ export class AgentTask<ResultT = unknown, UserData = any> extends Agent<UserData
       blockedTasks.push(onEnterTask);
     }
 
+    const activeRunState = session._globalRunState;
+    if (activeRunState && !activeRunState.done()) {
+      for (const task of blockedTasks) {
+        activeRunState._watchHandle(task);
+      }
+    }
+
     if (
       taskInfo.functionCall &&
       oldActivity.llm instanceof RealtimeModel &&
@@ -695,6 +702,8 @@ export class AgentTask<ResultT = unknown, UserData = any> extends Agent<UserData
       );
     }
 
+    const suspendedHandles: Array<SpeechHandle | Task<void>> = [];
+
     await session._updateActivity(this, {
       previousActivity: 'pause',
       newActivity: 'start',
@@ -702,16 +711,26 @@ export class AgentTask<ResultT = unknown, UserData = any> extends Agent<UserData
     });
 
     let runState = session._globalRunState;
-    if (speechHandle && runState && !runState.done()) {
-      // Only unwatch the parent speech handle if there are other handles keeping the run alive.
-      // When watchedHandleCount is 1 (only the parent), unwatching would drop it to 0 and
-      // mark the run done prematurely — before function_call_output and assistant message arrive.
-      if (runState._watchedHandleCount() > 1) {
-        runState._unwatchHandle(speechHandle);
+    if (runState && !runState.done()) {
+      if (speechHandle && runState._unwatchHandle(speechHandle)) {
+        suspendedHandles.push(speechHandle);
+      }
+
+      for (const task of blockedTasks) {
+        if (runState._unwatchHandle(task)) {
+          suspendedHandles.push(task);
+        }
+      }
+
+      // It is OK to call _markDoneIfNeeded here: _updateActivity has started
+      // the AgentTask activity, and any onEnter-generated speech is now watched.
+      // Only call it when something was actually suspended — a run created
+      // mid-transition has no watched handles yet (its generateReply is still
+      // deferred behind the activity lock), and marking done on an empty
+      // handle set would resolve it before it produced any events.
+      if (suspendedHandles.length > 0) {
+        runState._markDoneIfNeeded();
       }
-      // it is OK to call _markDoneIfNeeded here, the above _updateActivity will call onEnter
-      // and newly added handles keep the run alive.
-      runState._markDoneIfNeeded();
     }
 
     try {
@@ -727,8 +746,10 @@ export class AgentTask<ResultT = unknown, UserData = any> extends Agent<UserData
         );
         await oldActivity.close();
       } else {
-        if (speechHandle && runState && !runState.done()) {
-          runState._watchHandle(speechHandle);
+        if (runState && !runState.done()) {
+          for (const handle of suspendedHandles) {
+            runState._watchHandle(handle);
+          }
         }
 
         const mergedChatCtx = oldAgent._chatCtx.merge(this._chatCtx, {
diff --git a/agents/src/voice/agent_task_prerun_handoff.test.ts b/agents/src/voice/agent_task_prerun_handoff.test.ts
new file mode 100644
index 000000000..a7b15594a
--- /dev/null
+++ b/agents/src/voice/agent_task_prerun_handoff.test.ts
@@ -0,0 +1,135 @@
+// SPDX-FileCopyrightText: 2026 LiveKit, Inc.
+//
+// SPDX-License-Identifier: Apache-2.0
+//
+// Regression test for AgentTask handoffs triggered by a speech that predates
+// the active run (livekit/agents#6313, ported from livekit/agents#6315).
+//
+// When AgentSession.start() runs onEnter and its reply calls a tool that
+// awaits an AgentTask, nothing watches the tasks driving that handoff. The
+// first session.run() then completes as soon as its own reply finishes —
+// while the handoff is still mid-transition — and the run hangs or the next
+// run races the transition. The fix watches the blocked handoff tasks on the
+// active run for the duration of the activity transition.
+//
+// Without the fix, run('hi') below never resolves (the session stalls
+// mid-handoff) and the test times out.
+// Ref: python tests/test_nested_agent_task.py - test_handoff_from_pre_run_speech
+import { describe, expect, it } from 'vitest';
+import { tool } from '../llm/tool_context.js';
+import { initializeLogger } from '../log.js';
+import { Agent, AgentTask } from './agent.js';
+import { AgentSession } from './agent_session.js';
+import { FakeLLM } from './testing/fake_llm.js';
+
+let taskOnEnterCompletedAt = 0;
+
+class SimpleTask extends AgentTask<null> {
+  constructor() {
+    super({
+      instructions: 'simple task',
+      tools: [
+        tool({
+          name: 'finish',
+          description: 'Called to complete the task.',
+          execute: async () => {
+            this.complete(null);
+            return 'done';
+          },
+        }),
+      ],
+    });
+  }
+
+  async onEnter(): Promise<void> {
+    // Widen the mid-transition window (old activity paused, new activity
+    // still starting) so a run completing early is deterministically caught.
+    await new Promise((r) => setTimeout(r, 500));
+    this.session.generateReply({ userInput: 'task_greeting' });
+    taskOnEnterCompletedAt = Date.now();
+  }
+}
+
+class EnterHandoffAgent extends Agent {
+  constructor() {
+    super({
+      instructions: 'root agent',
+      tools: [
+        tool({
+          name: 'start_task',
+          description: 'Transitions into SimpleTask.',
+          execute: async () => {
+            await new SimpleTask().run();
+            return 'task completed';
+          },
+        }),
+      ],
+    });
+  }
+
+  async onEnter(): Promise<void> {
+    // This speech predates any session.run(), so no run watches it.
+    const handle = this.session.generateReply({ userInput: 'enter_greeting' });
+    await handle.waitForPlayout();
+  }
+}
+
+function withTimeout<T>(p: Promise<T>, ms: number, label: string): Promise<T> {
+  return Promise.race([
+    p,
+    new Promise<T>((_, reject) =>
+      setTimeout(() => reject(new Error(`timed out waiting for ${label}`)), ms),
+    ),
+  ]);
+}
+
+describe('AgentTask handoff from pre-run speech', () => {
+  initializeLogger({ pretty: false, level: 'silent' });
+
+  it('keeps the run alive until the handoff settles', async () => {
+    const llm = new FakeLLM([
+      // onEnter reply -> calls start_task; slow enough that run('hi') starts
+      // before the tool call lands
+      {
+        input: 'enter_greeting',
+        content: '',
+        ttft: 1000,
+        duration: 1000,
+        toolCalls: [{ name: 'start_task', args: {} }],
+      },
+      // user says "hi" while the handoff is in flight; the only speech the
+      // first run watches on its own
+      { input: 'hi', content: 'hello!', ttft: 1000, duration: 2000 },
+      // SimpleTask onEnter greeting
+      { input: 'task_greeting', content: 'hello from task' },
+      // user says "bye" -> LLM calls finish
+      {
+        input: 'bye',
+        content: '',
+        toolCalls: [{ name: 'finish', args: {} }],
+      },
+      // after start_task tool output, LLM responds
+      { input: 'task completed', content: 'all done' },
+    ]);
+
+    const session = new AgentSession({ llm });
+
+    try {
+      await session.start({ agent: new EnterHandoffAgent() });
+
+      await withTimeout(session.run({ userInput: 'hi' }).wait(), 10_000, "run('hi')");
+      const runResolvedAt = Date.now();
+      expect(session.currentAgent).toBeInstanceOf(SimpleTask);
+
+      // the run must not complete mid-handoff: the new activity's onEnter
+      // must already have finished when the run resolves
+      expect(taskOnEnterCompletedAt).toBeGreaterThan(0);
+      expect(runResolvedAt).toBeGreaterThanOrEqual(taskOnEnterCompletedAt);
+
+      await withTimeout(session.run({ userInput: 'bye' }).wait(), 10_000, "run('bye')");
+      expect(session.currentAgent).toBeInstanceOf(EnterHandoffAgent);
+    } finally {
+      await session.close().catch(() => {});
+    }
+  }, 30_000);
+});
diff --git a/agents/src/voice/testing/run_result.ts b/agents/src/voice/testing/run_result.ts
index 21c3a9e11..4033c9436 100644
--- a/agents/src/voice/testing/run_result.ts
+++ b/agents/src/voice/testing/run_result.ts
@@ -195,8 +195,8 @@ export class RunResult<T = unknown> {
    * @internal
    * Unwatch a handle.
    */
-  _unwatchHandle(handle: SpeechHandle | Task<void>): void {
-    this.handles.delete(handle);
+  _unwatchHandle(handle: SpeechHandle | Task<void>): boolean {
+    const wasWatched = this.handles.delete(handle);
     const doneCallback = this.doneCallbacks.get(handle);
 
     if (doneCallback) {
@@ -207,6 +207,8 @@ export class RunResult<T = unknown> {
     if (isSpeechHandle(handle)) {
       handle._removeItemAddedCallback(this.itemAddedCallback);
     }
+
+    return wasWatched;
   }
 
   /** @internal */