diff --git a/tests/runner-e2e/catalog.test.ts b/tests/runner-e2e/catalog.test.ts
index 969b43626cc..6a37e2ab92f 100644
--- a/tests/runner-e2e/catalog.test.ts
+++ b/tests/runner-e2e/catalog.test.ts
@@ -357,7 +357,7 @@ describe("runner E2E catalog", () => {
         (total, execution) => total + execution.task.expectedRunCount,
         0,
       ),
-    ).toBe(385);
+    ).toBe(397);
     expect(
       runnerTasks.find((task) => task.id === "plan-revise-accept")
         ?.attemptTimeoutMs,
diff --git a/tests/runner-e2e/chat-cases.ts b/tests/runner-e2e/chat-cases.ts
index 50d22658b4e..3684c003be2 100644
--- a/tests/runner-e2e/chat-cases.ts
+++ b/tests/runner-e2e/chat-cases.ts
@@ -15,9 +15,10 @@ export const CHAT_CASES = [
   ["continuity-restart", "Conversation continuity across restart", 3],
   ["new-session", "Fresh context within preserved history", 2],
   ["stop-new-resume", "Stop, reset, and resume", 3],
-  ["plan-handoff", "Draft, revise, approve, and hand off a plan", 4],
-  ["clarify-reuse", "Clarify and reuse an existing project", 3],
-  ["multi-repository", "Create a project with multiple repository URLs", 2],
+  // Handoff cases include the source chat's one completion-reply turn.
+  ["plan-handoff", "Draft, revise, approve, and hand off a plan", 5],
+  ["clarify-reuse", "Clarify and reuse an existing project", 4],
+  ["multi-repository", "Create a project with multiple repository URLs", 3],
 ] as const;
 export type ChatCase = (typeof CHAT_CASES)[number][0];
 const HARDENING_CASES = [
diff --git a/tests/runner-e2e/chat-flow.ts b/tests/runner-e2e/chat-flow.ts
index a5a76a5a5ff..0a8808fb826 100644
--- a/tests/runner-e2e/chat-flow.ts
+++ b/tests/runner-e2e/chat-flow.ts
@@ -183,6 +183,12 @@ export async function readChatOutputDocument(
 export const isResetRun = (run: ChatRun) =>
   run.contextSnapshot?.conversationReset === true ||
   run.resultJson?.conversationReset === true;
+/** The source chat's automatic turn that reports one completed handoff. */
+export const isChatCompletionReply = (run: ChatRun, chatIssueId: string, taskId: string) =>
+  run.contextSnapshot?.issueId === chatIssueId &&
+  run.contextSnapshot?.wakeReason === "chat_task_completed" &&
+  Array.isArray(run.contextSnapshot?.chatCompletionUpdates) &&
+  (run.contextSnapshot.chatCompletionUpdates as Array<{ id?: unknown }>).some((update) => update?.id === taskId);
 export function chatRunFailure(
   runs: ChatRun[],
   allowCancelled = false,
@@ -944,7 +950,28 @@ export async function runChatFlow(input: ChatFlowInput) {
         accept: (state) => state.task.status === "done",
         reject: (state) => chatTaskCompletionFailure(state.task, state.runs),
       });
-      runs = await allRuns();
+      // A completed handoff returns to the source chat (#14408) as one
+      // correlated provider turn. Observe that delivery instead of racing it.
+      const completionReply = await pollUntil({
+        label: `completion of ${child.id} is reported in the chat`,
+        deadlineAt: Date.now() + 240_000,
+        intervalMs: 1000,
+        load: async () => {
+          const rows = await allRuns();
+          const reply = rows.filter((run) => isChatCompletionReply(run, issue!.id, child.id));
+          return { runs: rows, reply, comments: await comments() };
+        },
+        // A native reply comment is presented after its run succeeds, so wait
+        // for the comment too; a failed reply turn settles immediately.
+        accept: (state) => state.reply.length > 0 &&
+          state.reply.every((run) => ["succeeded", "failed", "cancelled", "timed_out"].includes(run.status)) &&
+          (state.reply.some((run) => run.status !== "succeeded") ||
+            state.comments.some((c) => c.authorAgentId === f.agent.id && state.reply.some((run) => run.id === c.createdByRunId))),
+      });
+      expect(completionReply.reply.map((run) => run.status), "one completion reply turn").toEqual(["succeeded"]);
+      expect(completionReply.comments.filter((c) => c.authorAgentId === f.agent.id &&
+        c.createdByRunId === completionReply.reply[0]!.id), "completion reply posted in the chat").toHaveLength(1);
+      runs = completionReply.runs;
       input.observe(issue!, runs);
       const plan =
         caseId === "plan-handoff"
diff --git a/tests/runner-e2e/continuation-flow.ts b/tests/runner-e2e/continuation-flow.ts
index df999ff2537..06a8b3f6f12 100644
--- a/tests/runner-e2e/continuation-flow.ts
+++ b/tests/runner-e2e/continuation-flow.ts
@@ -12,7 +12,7 @@ import { answerableRuntimeRunIds, isSingleClaudeQuestion } from "./runtime-quest
 import { expect, type Page } from "@playwright/test";
 import path from "node:path";
 import { continuationAnswerCommitted, continuationInitialReady, continuationCheckpointReady } from "./continuation-readiness.js";
-import { captureLoadedContinuation } from "./continuation-screenshot.js";
+import { captureLoadedContinuation, waitForTaskChatRendered } from "./continuation-screenshot.js";
 import { seedContinuationContext } from "./continuation-workspace.js";
 import { pollUntil, type RunnerApi } from "./api.js";
 import {
@@ -130,10 +130,13 @@ export async function runContinuationFlow(input: {
     });
   }
   async function open() {
+    // A restarted dev server can leave DOMContentLoaded pending after the app
+    // is interactive (see chat-flow). Require the rendered task thread instead.
     await page.goto(
       `/${fixtures.company.issuePrefix}/issues/${issue!.identifier ?? issue!.id}`,
-      { waitUntil: "domcontentloaded" },
+      { waitUntil: "commit", timeout: 60_000 },
     );
+    await waitForTaskChatRendered(page, undefined, 60_000);
   }
   async function snapshot(phase: ContinuationCheckpoint["phase"]) {
     const [tasks, summaries, comments, interactions, attachments, activity] =