diff --git a/Sources/ContainerXPC/XPCClient.swift b/Sources/ContainerXPC/XPCClient.swift
index bab008509..ea4edb7e5 100644
--- a/Sources/ContainerXPC/XPCClient.swift
+++ b/Sources/ContainerXPC/XPCClient.swift
@@ -111,15 +111,19 @@ extension XPCClient {
             }
 
             group.addTask {
-                try await withCheckedThrowingContinuation { cont in
-                    xpc_connection_send_message_with_reply(self.connection, message.underlying, nil) { reply in
-                        do {
-                            let message = try self.parseReply(reply)
-                            cont.resume(returning: message)
-                        } catch {
-                            cont.resume(throwing: error)
+                let box = XPCReplyBox()
+                return try await withTaskCancellationHandler {
+                    try await withCheckedThrowingContinuation { cont in
+                        box.store(cont)
+                        xpc_connection_send_message_with_reply(self.connection, message.underlying, nil) { reply in
+                            box.resume { try self.parseReply(reply) }
                         }
                     }
+                } onCancel: {
+                    // On timeout the group cancels this task. The XPC reply
+                    // handler is not cancellation-aware, so resume the
+                    // continuation here; a late reply becomes a no-op.
+                    box.resume { throw CancellationError() }
                 }
             }
 
diff --git a/Sources/ContainerXPC/XPCReplyBox.swift b/Sources/ContainerXPC/XPCReplyBox.swift
new file mode 100644
index 000000000..24a9a1c07
--- /dev/null
+++ b/Sources/ContainerXPC/XPCReplyBox.swift
@@ -0,0 +1,68 @@
+//===----------------------------------------------------------------------===//
+// Copyright © 2026 Apple Inc. and the container project authors.
+//
+// Licensed under the Apache License, Version 2.0 (the "License");
+// you may not use this file except in compliance with the License.
+// You may obtain a copy of the License at
+//
+//   https://www.apache.org/licenses/LICENSE-2.0
+//
+// Unless required by applicable law or agreed to in writing, software
+// distributed under the License is distributed on an "AS IS" BASIS,
+// WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+// See the License for the specific language governing permissions and
+// limitations under the License.
+//===----------------------------------------------------------------------===//
+
+#if os(macOS)
+import Foundation
+
+/// Resume-once bridge between a `CheckedContinuation` and the XPC reply handler.
+///
+/// The XPC reply handler is not cancellation-aware, so a request can outlive a
+/// client-side timeout. This box lets either the reply handler or the task's
+/// cancellation handler resume the continuation, whichever fires first, while
+/// guaranteeing it is resumed exactly once. A continuation resumed twice traps.
+final class XPCReplyBox: @unchecked Sendable {
+    private let lock = NSLock()
+    private var cont: CheckedContinuation<XPCMessage, Error>?
+    private var resumed = false
+    private var pending: Result<XPCMessage, Error>?
+
+    /// Store the continuation. If a resume already raced ahead (cancellation
+    /// before the continuation was installed), honor it immediately.
+    func store(_ cont: CheckedContinuation<XPCMessage, Error>) {
+        lock.lock()
+        if let pending, !resumed {
+            resumed = true
+            lock.unlock()
+            cont.resume(with: pending)
+            return
+        }
+        self.cont = cont
+        lock.unlock()
+    }
+
+    /// Resume the continuation with the result of `body`, at most once. A later
+    /// call is a no-op, so the reply handler and the cancellation handler can
+    /// both call it safely.
+    func resume(_ body: () throws -> XPCMessage) {
+        let result = Result { try body() }
+        lock.lock()
+        guard !resumed else {
+            lock.unlock()
+            return
+        }
+        guard let cont else {
+            pending = result
+            lock.unlock()
+            return
+        }
+        resumed = true
+        self.cont = nil
+        lock.unlock()
+        cont.resume(with: result)
+    }
+}
+
+#endif
diff --git a/Sources/ContainerXPC/XPCServer.swift b/Sources/ContainerXPC/XPCServer.swift
index b33453142..a46dc0873 100644
--- a/Sources/ContainerXPC/XPCServer.swift
+++ b/Sources/ContainerXPC/XPCServer.swift
@@ -241,6 +241,16 @@ public struct XPCServer: Sendable {
                 }
                 xpc_connection_send_message(connection, reply.underlying)
             }
+        } else {
+            // No handler for this route: reply with an error instead of dropping
+            // the message, otherwise the client blocks until its timeout (or
+            // forever, if it sent none).
+            log.error("no handler registered for route", metadata: ["route": "\(route)"])
+            Self.replyWithError(
+                connection: connection,
+                object: object,
+                err: ContainerizationError(.invalidArgument, message: "unknown route: \(route)")
+            )
         }
     }