diff --git a/src/features/background-agent/manager.test.ts b/src/features/background-agent/manager.test.ts
index d81698cb5..c4db9056b 100644
--- a/src/features/background-agent/manager.test.ts
+++ b/src/features/background-agent/manager.test.ts
@@ -1123,6 +1123,99 @@ describe("BackgroundManager.tryCompleteTask", () => {
     expect(task.status).toBe("completed")
     expect(getPendingByParent(manager).get(task.parentSessionID)).toBeUndefined()
   })
+
+  test("should avoid overlapping promptAsync calls when tasks complete concurrently", async () => {
+    // given
+    type PromptAsyncBody = Record<string, unknown> & { noReply?: boolean }
+
+    let resolveMessages: ((value: { data: unknown[] }) => void) | undefined
+    const messagesBarrier = new Promise<{ data: unknown[] }>((resolve) => {
+      resolveMessages = resolve
+    })
+
+    const promptBodies: PromptAsyncBody[] = []
+    let promptInFlight = false
+    let rejectedCount = 0
+    let promptCallCount = 0
+
+    let releaseFirstPrompt: (() => void) | undefined
+    let resolveFirstStarted: (() => void) | undefined
+    const firstStarted = new Promise<void>((resolve) => {
+      resolveFirstStarted = resolve
+    })
+
+    const client = {
+      session: {
+        prompt: async () => ({}),
+        abort: async () => ({}),
+        messages: async () => messagesBarrier,
+        promptAsync: async (args: { path: { id: string }; body: PromptAsyncBody }) => {
+          promptBodies.push(args.body)
+
+          if (!promptInFlight) {
+            promptCallCount += 1
+            if (promptCallCount === 1) {
+              promptInFlight = true
+              resolveFirstStarted?.()
+              return await new Promise((resolve) => {
+                releaseFirstPrompt = () => {
+                  promptInFlight = false
+                  resolve({})
+                }
+              })
+            }
+
+            return {}
+          }
+
+          rejectedCount += 1
+          throw new Error("BUSY")
+        },
+      },
+    }
+
+    manager.shutdown()
+    manager = new BackgroundManager({ client, directory: tmpdir() } as unknown as PluginInput)
+
+    const parentSessionID = "parent-session"
+    const taskA = createMockTask({
+      id: "task-a",
+      sessionID: "session-a",
+      parentSessionID,
+    })
+    const taskB = createMockTask({
+      id: "task-b",
+      sessionID: "session-b",
+      parentSessionID,
+    })
+
+    getTaskMap(manager).set(taskA.id, taskA)
+    getTaskMap(manager).set(taskB.id, taskB)
+    getPendingByParent(manager).set(parentSessionID, new Set([taskA.id, taskB.id]))
+
+    // when
+    const completionA = tryCompleteTaskForTest(manager, taskA)
+    const completionB = tryCompleteTaskForTest(manager, taskB)
+    resolveMessages?.({ data: [] })
+
+    await firstStarted
+
+    // Give the second completion a chance to attempt promptAsync while the first is in-flight.
+    // In the buggy implementation, this triggers an overlap and increments rejectedCount.
+    for (let i = 0; i < 20; i++) {
+      await Promise.resolve()
+      if (rejectedCount > 0) break
+      if (promptBodies.length >= 2) break
+    }
+
+    releaseFirstPrompt?.()
+    await Promise.all([completionA, completionB])
+
+    // then
+    expect(rejectedCount).toBe(0)
+    expect(promptBodies.length).toBe(2)
+    expect(promptBodies.some((b) => b.noReply === false)).toBe(true)
+  })
 })
 
 describe("BackgroundManager.trackTask", () => {
diff --git a/src/features/background-agent/manager.ts b/src/features/background-agent/manager.ts
index e631f30a0..0604c876b 100644
--- a/src/features/background-agent/manager.ts
+++ b/src/features/background-agent/manager.ts
@@ -89,6 +89,7 @@ export class BackgroundManager {
   private processingKeys: Set<string> = new Set()
   private completionTimers: Map<string, ReturnType<typeof setTimeout>> = new Map()
   private idleDeferralTimers: Map<string, ReturnType<typeof setTimeout>> = new Map()
+  private notificationQueueByParent: Map<string, Promise<void>> = new Map()
 
   constructor(
     ctx: PluginInput,
@@ -358,7 +359,7 @@ export class BackgroundManager {
 
         this.markForNotification(existingTask)
         this.cleanupPendingByParent(existingTask)
-        this.notifyParentSession(existingTask).catch(err => {
+        this.enqueueNotificationForParent(existingTask.parentSessionID, () => this.notifyParentSession(existingTask)).catch(err => {
           log("[background-agent] Failed to notify on error:", err)
         })
       }
@@ -615,7 +616,7 @@ export class BackgroundManager {
 
       this.markForNotification(existingTask)
       this.cleanupPendingByParent(existingTask)
-      this.notifyParentSession(existingTask).catch(err => {
+      this.enqueueNotificationForParent(existingTask.parentSessionID, () => this.notifyParentSession(existingTask)).catch(err => {
         log("[background-agent] Failed to notify on resume error:", err)
       })
     })
@@ -949,7 +950,7 @@ export class BackgroundManager {
     this.markForNotification(task)
 
     try {
-      await this.notifyParentSession(task)
+      await this.enqueueNotificationForParent(task.parentSessionID, () => this.notifyParentSession(task))
       log(`[background-agent] Task cancelled via ${source}:`, task.id)
     } catch (err) {
       log("[background-agent] Error in notifyParentSession for cancelled task:", { taskId: task.id, error: err })
@@ -1084,7 +1085,7 @@ export class BackgroundManager {
     }
 
     try {
-      await this.notifyParentSession(task)
+      await this.enqueueNotificationForParent(task.parentSessionID, () => this.notifyParentSession(task))
       log(`[background-agent] Task completed via ${source}:`, task.id)
     } catch (err) {
       log("[background-agent] Error in notifyParentSession:", { taskId: task.id, error: err })
@@ -1114,16 +1115,19 @@ export class BackgroundManager {
 
     // Update pending tracking and check if all tasks complete
     const pendingSet = this.pendingByParent.get(task.parentSessionID)
+    let allComplete = false
+    let remainingCount = 0
     if (pendingSet) {
       pendingSet.delete(task.id)
-      if (pendingSet.size === 0) {
+      remainingCount = pendingSet.size
+      allComplete = remainingCount === 0
+      if (allComplete) {
         this.pendingByParent.delete(task.parentSessionID)
       }
+    } else {
+      allComplete = true
     }
 
-    const allComplete = !pendingSet || pendingSet.size === 0
-    const remainingCount = pendingSet?.size ?? 0
-
     const statusText = task.status === "completed" ? "COMPLETED" : "CANCELLED"
     const errorInfo = task.error ? `\n**Error:** ${task.error}` : ""
     
@@ -1378,7 +1382,7 @@ Use \`background_output(task_id="${task.id}")\` to retrieve this result when rea
       log(`[background-agent] Task ${task.id} interrupted: stale timeout`)
 
       try {
-        await this.notifyParentSession(task)
+        await this.enqueueNotificationForParent(task.parentSessionID, () => this.notifyParentSession(task))
       } catch (err) {
         log("[background-agent] Error in notifyParentSession for stale task:", { taskId: task.id, error: err })
       }
@@ -1572,12 +1576,37 @@ Use \`background_output(task_id="${task.id}")\` to retrieve this result when rea
     this.tasks.clear()
     this.notifications.clear()
     this.pendingByParent.clear()
+    this.notificationQueueByParent.clear()
     this.queuesByKey.clear()
     this.processingKeys.clear()
     this.unregisterProcessCleanup()
     log("[background-agent] Shutdown complete")
 
   }
+
+  private enqueueNotificationForParent(
+    parentSessionID: string | undefined,
+    operation: () => Promise<void>
+  ): Promise<void> {
+    if (!parentSessionID) {
+      return operation()
+    }
+
+    const previous = this.notificationQueueByParent.get(parentSessionID) ?? Promise.resolve()
+    const current = previous
+      .catch(() => {})
+      .then(operation)
+
+    this.notificationQueueByParent.set(parentSessionID, current)
+
+    void current.finally(() => {
+      if (this.notificationQueueByParent.get(parentSessionID) === current) {
+        this.notificationQueueByParent.delete(parentSessionID)
+      }
+    }).catch(() => {})
+
+    return current
+  }
 }
 
 function registerProcessSignal(