diff --git a/src/auto-reply/inbound-debounce.ts b/src/auto-reply/inbound-debounce.ts
index b5eb48e9fed9..63f93fe1c3f0 100644
--- a/src/auto-reply/inbound-debounce.ts
+++ b/src/auto-reply/inbound-debounce.ts
@@ -127,13 +127,13 @@ function createInboundDebounceFlush(params: {
   }
   // A failed dispatch must settle its source claim before releasing the keyed
   // lane; an already-admitted turn owns its later completion failure.
-  void completion
-    .then(markAdmitted, async (error: unknown) => {
-      if (!admitted) {
-        await lifecycle.onFailed?.(error);
-      }
-    })
-    .then(markAdmitted, markAdmitted);
+  completion = completion.then(markAdmitted).catch(async (error: unknown) => {
+    if (!admitted && lifecycle.onFailed) {
+      await Promise.allSettled([lifecycle.onFailed(error)]);
+    }
+    markAdmitted();
+    throw error;
+  });
   return { admission, completion };
 }
 
@@ -197,7 +197,7 @@ export function createInboundDebouncer<T>(params: InboundDebounceCreateParams<T>
     activeCompletions.add(completion);
     const cleanup = () => activeCompletions.delete(completion);
     void completion.then(cleanup, cleanup);
-    await admission;
+    await Promise.race([admission, completion]);
   };
 
   const cancelItems = (items: T[]) => {
diff --git a/src/auto-reply/inbound.test.ts b/src/auto-reply/inbound.test.ts
index 9e8c612c5516..06d74ca05c26 100644
--- a/src/auto-reply/inbound.test.ts
+++ b/src/auto-reply/inbound.test.ts
@@ -1008,6 +1008,45 @@ describe("createInboundDebouncer", () => {
     expect(calls).toEqual(["1", "2"]);
   });
 
+  it("releases serialized keys when custom completion rejects before admission", async () => {
+    const failure = new Error("custom flush failed");
+    const calls: string[] = [];
+    const reported: unknown[] = [];
+    const pendingAdmission = new Promise<void>(() => {});
+    const debouncer = createInboundDebouncer<{ key: string; id: string }>({
+      debounceMs: 0,
+      serializeImmediate: true,
+      buildKey: (item) => item.key,
+      onFlush: (items) => {
+        const id = items[0]?.id ?? "";
+        calls.push(id);
+        if (id === "first") {
+          return { admission: pendingAdmission, completion: Promise.reject(failure) };
+        }
+        return flushOnCompletion(() => {});
+      },
+      onError: (error) => {
+        reported.push(error);
+        throw new Error("observer failed");
+      },
+    });
+
+    const first = debouncer.enqueue({ key: "a", id: "first" });
+    await vi.waitFor(() => expect(calls).toEqual(["first"]));
+    const second = debouncer.enqueue({ key: "a", id: "second" });
+    const secondOutcome = await Promise.race([
+      second.then(() => "completed" as const),
+      new Promise<"stalled">((resolve) => {
+        setTimeout(() => resolve("stalled"), 100);
+      }),
+    ]);
+
+    expect(secondOutcome).toBe("completed");
+    await Promise.all([first, second, debouncer.drain()]);
+    expect(calls).toEqual(["first", "second"]);
+    expect(reported).toEqual([failure]);
+  });
+
   it("does not leak unhandled rejections when a keyed flush failure is awaited", async () => {
     const debouncer = createInboundDebouncer<{ key: string; id: string }>({
       debounceMs: 0,