diff --git a/static/messages.js b/static/messages.js
index ff496d19..daa2fdd1 100644
--- a/static/messages.js
+++ b/static/messages.js
@@ -8139,6 +8139,9 @@ let _approvalSSEHealthTimer = null;
 let _approvalPollingSessionId = null;
 // Session whose poller stopped on a profile-mismatch 409; re-armed on focus/visibility.
 let _approvalProfilePausedSessionId = null;
+// Bumped on every focus/visibility return. A mismatch 409 for a request that began before
+// the latest return may predate a cookie switch-back, so it earns one retry before pausing.
+let _promptPollerFocusEpoch = 0;
 
 function _startApprovalFallbackPoll(sid) {
   _approvalProfilePausedSessionId = null;
@@ -8151,6 +8154,7 @@ function _startApprovalFallbackPoll(sid) {
     }
     if (_approvalFallbackPollInFlight) return;
     _approvalFallbackPollInFlight = true;
+    const focusEpoch = _promptPollerFocusEpoch;
     try {
       const generation = _approvalPromptGeneration(sid);
       const data = await api("/api/approval/pending?session_id=" + encodeURIComponent(sid),{timeoutToast:false});
@@ -8172,8 +8176,9 @@ function _startApprovalFallbackPoll(sid) {
       // Only this poller may stop itself: a late 409 from a replaced poller must not kill its successor.
       if (typeof _sessionProfileMismatchFromError === 'function' && _sessionProfileMismatchFromError(e)
           && _approvalPollTimer === pollTimer) {
-        stopApprovalPolling();
-        _approvalProfilePausedSessionId = sid;
+        // Focus returned mid-request: the cookie may be back, so retry once (after finally).
+        if (focusEpoch !== _promptPollerFocusEpoch) queueMicrotask(_tick);
+        else { stopApprovalPolling(); _approvalProfilePausedSessionId = sid; }
       }
     }
     finally { if (_approvalPollTimer === pollTimer) _approvalFallbackPollInFlight = false; }
@@ -9337,6 +9342,7 @@ function _startClarifyFallbackPoll(sid) {
     }
     if (_clarifyFallbackPollInFlight) return;
     _clarifyFallbackPollInFlight = true;
+    const focusEpoch = _promptPollerFocusEpoch;
     try {
       const generation = _clarifyPromptGeneration(sid);
       const data = await api("/api/clarify/pending?session_id=" + encodeURIComponent(sid),{timeoutToast:false});
@@ -9363,8 +9369,8 @@ function _startClarifyFallbackPoll(sid) {
       // Only this poller may stop itself: a late 409 from a replaced poller must not kill its successor.
       if (typeof _sessionProfileMismatchFromError === "function" && _sessionProfileMismatchFromError(e)) {
         if (_clarifyFallbackTimer === pollTimer) {
-          stopClarifyPolling();
-          _clarifyProfilePausedSessionId = sid;
+          if (focusEpoch !== _promptPollerFocusEpoch) queueMicrotask(_tick);
+          else { stopClarifyPolling(); _clarifyProfilePausedSessionId = sid; }
         }
         return;
       }
@@ -9441,6 +9447,7 @@ function stopClarifyPolling() {
 // profile just 409s once and pauses them again.
 function _resumeProfilePausedPromptPollers() {
   if (typeof document !== 'undefined' && document.hidden) return;
+  _promptPollerFocusEpoch++;
   const current = (S.session && S.session.session_id) || null;
   const approvalSid = _approvalProfilePausedSessionId;
   const clarifySid = _clarifyProfilePausedSessionId;
diff --git a/tests/test_console_noise_git_info_and_pollers.py b/tests/test_console_noise_git_info_and_pollers.py
index 6132a49f..fa289434 100644
--- a/tests/test_console_noise_git_info_and_pollers.py
+++ b/tests/test_console_noise_git_info_and_pollers.py
@@ -124,6 +124,7 @@ var _clarifyEventSource = null, _clarifyFallbackTimer = null, _clarifyHealthTime
 var _clarifyFallbackPollInFlight = false, _clarifyPollingSessionId = null, _clarifyMissingEndpointWarned = false;
 var _approvalPendingBySession = new Map();
 var _approvalProfilePausedSessionId = null, _clarifyProfilePausedSessionId = null;
+var _promptPollerFocusEpoch = 0;
 function _approvalPromptGeneration(){ return 0; }
 function _clarifyPromptGeneration(){ return 0; }
 function _approvalPollingSessionMissingOrMismatched(sid){ return !sid || !S.session || S.session.session_id !== sid; }
@@ -335,3 +336,68 @@ process.stdout.write(String(started));
     out = subprocess.run([node, "-e", script], capture_output=True, text=True, timeout=30)
     assert out.returncode == 0, out.stderr
     assert out.stdout == "0"
+
+
+def _run_late_409_after_focus(kind, cookie_back):
+    """The request starts under the old profile, focus returns while it is in flight,
+    then the old-profile 409 lands. The poller must retry once under the current
+    cookie instead of pausing for good; it pauses only if the retry also mismatches."""
+    node = shutil.which("node")
+    if not node:
+        pytest.skip("node not installed")
+    approval = kind == "approval"
+    fns = [
+        _extract_fn(SESSIONS_JS, "_sessionProfileMismatchFromError"),
+        _extract_fn(MESSAGES_JS, "startApprovalPolling"),
+        _extract_fn(MESSAGES_JS, "_startApprovalFallbackPoll"),
+        _extract_fn(MESSAGES_JS, "stopApprovalPollingForSession"),
+        _extract_fn(MESSAGES_JS, "stopApprovalPolling"),
+        _extract_fn(MESSAGES_JS, "startClarifyPolling"),
+        _extract_fn(MESSAGES_JS, "_startClarifyFallbackPoll"),
+        _extract_fn(MESSAGES_JS, "stopClarifyPollingForSession"),
+        _extract_fn(MESSAGES_JS, "stopClarifyPolling"),
+        _extract_fn(MESSAGES_JS, "_resumeProfilePausedPromptPollers"),
+    ]
+    harness = _HARNESS.replace("STATUS", "409").replace("BODY", json.dumps(_MISMATCH))
+    harness = harness.replace("async function api(){", """var mismatch = true, releaseFirst = null;
+async function api(){
+  if (!releaseFirst) { await new Promise(r => { releaseFirst = r; }); return _mismatchThrow(); }
+  if (!mismatch) { calls.api++; return {pending: {id: 'p1'}}; }
+  return _mismatchThrow();
+}
+function _mismatchThrow(){""")
+    harness = harness.replace("function showApprovalForSession(){}", "function showApprovalForSession(){ calls.shown = (calls.shown||0) + 1; }")
+    harness = harness.replace("function showClarifyForSession(){}", "function showClarifyForSession(){ calls.shown = (calls.shown||0) + 1; }")
+    start = "startApprovalPolling" if approval else "startClarifyPolling"
+    timer = "_approvalPollTimer" if approval else "_clarifyFallbackTimer"
+    script = harness + "\n".join(fns) + f"""
+const tick = () => new Promise(r => setTimeout(r, 0));
+(async () => {{
+  {start}('sid1');
+  await tick();                          // first request is in flight under the old cookie
+  mismatch = {'false' if cookie_back else 'true'};   // other tab switches the cookie (back or not)
+  _resumeProfilePausedPromptPollers();   // focus returns: nothing paused yet, so nothing to restart
+  releaseFirst();                        // the late old-profile 409 lands
+  for (let i = 0; i < 5; i++) await tick();
+  process.stdout.write(JSON.stringify({{api: calls.api, shown: calls.shown || 0,
+    running: {timer} !== null}}));
+}})();
+"""
+    out = subprocess.run([node, "-e", script], capture_output=True, text=True, timeout=30)
+    assert out.returncode == 0, out.stderr
+    return json.loads(out.stdout)
+
+
+@pytest.mark.parametrize("kind", ["approval", "clarify"])
+def test_late_409_after_focus_retries_once_and_shows_pending(kind):
+    r = _run_late_409_after_focus(kind, cookie_back=True)
+    assert r["api"] == 2, "a 409 for a request that predates focus must be retried once"
+    assert r["shown"] == 1, "the pending prompt must be shown after the retry"
+    assert r["running"] is True, "polling must keep running after the successful retry"
+
+
+@pytest.mark.parametrize("kind", ["approval", "clarify"])
+def test_late_409_after_focus_pauses_when_retry_still_mismatches(kind):
+    r = _run_late_409_after_focus(kind, cookie_back=False)
+    assert r["shown"] == 0
+    assert r["running"] is False, "a retry that still mismatches must pause, not loop"
diff --git a/tests/test_prompt_notification_lifecycle.py b/tests/test_prompt_notification_lifecycle.py
index 137e145e..6257e45a 100644
--- a/tests/test_prompt_notification_lifecycle.py
+++ b/tests/test_prompt_notification_lifecycle.py
@@ -24,6 +24,7 @@ const S = {busy:true,session:{session_id:'s'}};
 const _approvalPromptBelongsToActiveSession=()=>false;
 let _approvalSessionId = 's', _approvalCurrentId = 'id';
 let _approvalFallbackPollInFlight=false, _approvalPollTimer;
+let _promptPollerFocusEpoch=0;
 let _clarifyPollingSessionId, _clarifyPollTimer, _clarifyFallbackPollInFlight=false;
 const _promptActiveSessionId=()=> 's';
 const _approvalPollingSessionMissingOrMismatched=()=>false;