diff --git a/packages/api/src/schedules/fire.spec.ts b/packages/api/src/schedules/fire.spec.ts
index 76bf1a5787..db328db297 100644
--- a/packages/api/src/schedules/fire.spec.ts
+++ b/packages/api/src/schedules/fire.spec.ts
@@ -281,6 +281,28 @@ describe('fireSchedule', () => {
     expect(calls.advance).toBe(1);
   });
 
+  it('treats a message-limiter 429 as a skip, not a schedule failure', async () => {
+    const { methods, runs } = makeMethods();
+    mockFetch(
+      async () =>
+        ({
+          ok: false,
+          status: 429,
+          text: async () => '{"message":"Too many requests"}',
+        }) as Response,
+    );
+    const result = await fireSchedule(makeDeps(methods), makeSchedule(), LIMITS, dueAt(), {
+      manual: true,
+    });
+    expect(result.skipped).toBe('rate_limited');
+    // Counting this as a failure would let an owner merely over their message quota
+    // auto-disable a healthy schedule by clicking Run Now enough times.
+    expect(methods.recordRunOutcome).not.toHaveBeenCalled();
+    // Nothing reached the controller, so no outcome was recorded for the occurrence and
+    // the reservation must not be left holding its capacity slot.
+    expect([...runs.values()].filter((r) => r.status === 'started')).toHaveLength(0);
+  });
+
   it('records a definite HTTP rejection as error', async () => {
     const { methods, calls } = makeMethods();
     mockFetch(async () => ({ ok: false, status: 500, text: async () => 'boom' }) as Response);
diff --git a/packages/api/src/schedules/fire.ts b/packages/api/src/schedules/fire.ts
index 65bc3ec547..bfdfbb5e1f 100644
--- a/packages/api/src/schedules/fire.ts
+++ b/packages/api/src/schedules/fire.ts
@@ -27,6 +27,11 @@ class ScheduleFireError extends Error {
      *  controller already recorded the occurrence's outcome — so this is a SKIP, not a
      *  fault, and must not count toward auto-disable. */
     readonly preStartAbort = false,
+    /** The server's own message limiter refused the fire before it reached the
+     *  controller. Reachable for a manual Run Now, which is deliberately NOT exempt from
+     *  the interactive limiters. Nothing started and the schedule is not at fault, so
+     *  this must not count toward auto-disable either. */
+    readonly throttled = false,
   ) {
     super(message);
   }
@@ -162,10 +167,15 @@ async function postChatMessageInner(
   }
   if (!response.ok) {
     const body = await response.text().catch(() => '');
-    // A received error response is a definite rejection (nothing started).
+    // A received error response is a definite rejection (nothing started). 429 is the
+    // exception: the server's OWN message limiter refused the request, which says
+    // nothing about the schedule's health. Only a manual Run Now can reach it, since
+    // automatic occurrences are exempt.
     throw new ScheduleFireError(
       `Fire POST failed (${response.status}): ${body.slice(0, 300)}`,
       false,
+      false,
+      response.status === 429,
     );
   }
   // The accept path always answers with JSON ({ streamId, conversationId, status }).
@@ -530,6 +540,19 @@ export async function fireSchedule(
         await advance();
         return { fired: false, skipped: 'superseded' as const };
       }
+      if (error instanceof ScheduleFireError && error.throttled) {
+        // The server's own message limiter refused this before it reached the
+        // controller, so nothing was billed and the SCHEDULE is not at fault. Counting
+        // it as a failure would let an owner who is merely over their message quota
+        // auto-disable a perfectly healthy schedule by clicking Run Now enough times.
+        // Unlike the controller fence above, nothing recorded an outcome for this
+        // occurrence, so the reservation has to be rolled back or it holds its capacity
+        // slot and blocks overlap until the orphan sweep.
+        logger.info(`[schedules] fire refused by the message limiter for ${schedule.id}`);
+        await rollbackReservation();
+        await advance();
+        return { fired: false, skipped: 'rate_limited' as const };
+      }
       // Definite rejection (an error response was received): nothing started.
       logger.error(`[schedules] fire rejected for ${schedule.id}:`, error);
       await methods.recordRunOutcome({
diff --git a/packages/api/src/schedules/handlers.ts b/packages/api/src/schedules/handlers.ts
index cb040635c5..9dd88ebed7 100644
--- a/packages/api/src/schedules/handlers.ts
+++ b/packages/api/src/schedules/handlers.ts
@@ -412,8 +412,13 @@ export function createSchedulesHandlers(deps: SchedulesHandlersDeps): SchedulesH
       return;
     }
     if (!result.fired) {
-      res.status(409).json({
-        error: result.error ?? `Run skipped (${result.skipped ?? 'unknown'})`,
+      // A limiter refusal is the caller's own quota, not a conflicting schedule state,
+      // so answer 429 rather than burying it in the generic 409.
+      res.status(result.skipped === 'rate_limited' ? 429 : 409).json({
+        error:
+          result.skipped === 'rate_limited'
+            ? 'Too many messages. Try running this schedule again shortly.'
+            : (result.error ?? `Run skipped (${result.skipped ?? 'unknown'})`),
         skipped: result.skipped,
       });
       return;
diff --git a/packages/api/src/schedules/types.ts b/packages/api/src/schedules/types.ts
index f3d03c83df..0708b26d60 100644
--- a/packages/api/src/schedules/types.ts
+++ b/packages/api/src/schedules/types.ts
@@ -138,6 +138,7 @@ export interface FireResult {
     | 'user_missing'
     | 'user_deleting'
     | 'permission_revoked'
+    | 'rate_limited'
     | 'disabled';
   error?: string;
 }