diff --git a/src/agents/auth-profiles/usage.test.ts b/src/agents/auth-profiles/usage.test.ts
index 7ccdc9dd4b5..1dd20d03e81 100644
--- a/src/agents/auth-profiles/usage.test.ts
+++ b/src/agents/auth-profiles/usage.test.ts
@@ -812,6 +812,23 @@ describe("markAuthProfileFailure — per-model cooldown metadata", () => {
     expect(stats?.cooldownModel).toBe("claude-sonnet-4.6");
   });
 
+  it("widens cooldownModel when rate_limit failure during active cooldown has no modelId", async () => {
+    const now = 1_000_000;
+    const store = makeStoreWithCopilot({
+      "github-copilot:github": {
+        cooldownUntil: now + 30_000,
+        cooldownReason: "rate_limit",
+        cooldownModel: "claude-sonnet-4.6",
+        errorCount: 1,
+        lastFailureAt: now - 1000,
+      },
+    });
+    await markFailure({ store, now, modelId: undefined });
+    const stats = store.usageStats?.["github-copilot:github"];
+    expect(stats?.cooldownReason).toBe("rate_limit");
+    expect(stats?.cooldownModel).toBeUndefined();
+  });
+
   it("updates cooldownReason when auth failure occurs during active rate_limit window", async () => {
     const now = 1_000_000;
     const store = makeStoreWithCopilot({
diff --git a/src/agents/auth-profiles/usage.ts b/src/agents/auth-profiles/usage.ts
index f770d056e1d..8efa250ab5f 100644
--- a/src/agents/auth-profiles/usage.ts
+++ b/src/agents/auth-profiles/usage.ts
@@ -511,6 +511,14 @@ function computeNextProfileUsageStats(params: {
         params.existing.cooldownModel !== params.modelId
       ) {
         updatedStats.cooldownModel = undefined;
+      } else if (
+        params.reason === "rate_limit" &&
+        !params.modelId &&
+        params.existing.cooldownModel
+      ) {
+        // Unknown originating model during an active model-scoped cooldown:
+        // widen scope conservatively so no model can bypass on stale metadata.
+        updatedStats.cooldownModel = undefined;
       } else if (params.reason !== "rate_limit") {
         // Non-rate-limit failures are profile-wide — clear model scope even
         // when the same model fails, so that no model can bypass.
diff --git a/src/auto-reply/reply/agent-runner-execution.ts b/src/auto-reply/reply/agent-runner-execution.ts
index 1476986c3bb..75377bc67b5 100644
--- a/src/auto-reply/reply/agent-runner-execution.ts
+++ b/src/auto-reply/reply/agent-runner-execution.ts
@@ -83,13 +83,14 @@ export type AgentRunLoopResult =
  * Build a human-friendly rate-limit message from a FallbackSummaryError.
  * Includes a countdown when the soonest cooldown expiry is known.
  */
-function buildCopilotCooldownMessage(err: unknown): string {
+function buildRateLimitCooldownMessage(err: unknown): string {
   if (!isFallbackSummaryError(err)) {
     return "⚠️ All models are temporarily rate-limited. Please try again in a few minutes.";
   }
   const expiry = err.soonestCooldownExpiry;
-  if (typeof expiry === "number" && expiry > Date.now()) {
-    const secsLeft = Math.ceil((expiry - Date.now()) / 1000);
+  const now = Date.now();
+  if (typeof expiry === "number" && expiry > now) {
+    const secsLeft = Math.max(1, Math.ceil((expiry - now) / 1000));
     if (secsLeft <= 60) {
       return `⚠️ Rate-limited — ready in ~${secsLeft}s. Please wait a moment.`;
     }
@@ -702,7 +703,7 @@ export async function runAgentTurnWithFallback(params: {
       const fallbackText = isBilling
         ? BILLING_ERROR_USER_MESSAGE
         : isRateLimit
-          ? buildCopilotCooldownMessage(err)
+          ? buildRateLimitCooldownMessage(err)
           : isContextOverflow
             ? "⚠️ Context overflow — prompt too large for this model. Try a shorter message or a larger-context model."
             : isRoleOrderingError