diff --git a/native/computer-use-macos/Sources/OrcaComputerUseMacOS/main.swift b/native/computer-use-macos/Sources/OrcaComputerUseMacOS/main.swift
index da6c4d34cda..d7cd9204623 100644
--- a/native/computer-use-macos/Sources/OrcaComputerUseMacOS/main.swift
+++ b/native/computer-use-macos/Sources/OrcaComputerUseMacOS/main.swift
@@ -2530,9 +2530,12 @@ private enum KeyMap {
 }
 
 private final class AgentRuntime: NSObject, NSApplicationDelegate {
+    private static let unclaimedSessionDeadline: TimeInterval = 30
+
     private let socketPath: String
     private let token: String?
     private var listener: SocketListener?
+    private var unclaimedSessionTimeout: DispatchWorkItem?
 
     init(socketPath: String, token: String?) {
         self.socketPath = socketPath
@@ -2541,9 +2544,31 @@ private final class AgentRuntime: NSObject, NSApplicationDelegate {
 
     func applicationDidFinishLaunching(_ notification: Notification) {
         do {
-            let listener = try SocketListener(socketPath: socketPath, token: token)
+            let timeout = DispatchWorkItem {
+                fputs("computer-use agent received no authenticated session before its deadline\n", stderr)
+                NSApp.terminate(nil)
+            }
+            unclaimedSessionTimeout = timeout
+            let listener = try SocketListener(
+                socketPath: socketPath,
+                token: token,
+                onSessionClaimed: {
+                    DispatchQueue.main.async {
+                        timeout.cancel()
+                    }
+                },
+                onSessionClosed: {
+                    DispatchQueue.main.async {
+                        NSApp.terminate(nil)
+                    }
+                }
+            )
             self.listener = listener
             listener.start()
+            DispatchQueue.main.asyncAfter(
+                deadline: .now() + Self.unclaimedSessionDeadline,
+                execute: timeout
+            )
         } catch {
             fputs("failed to start computer-use socket: \(error)\n", stderr)
             NSApp.terminate(nil)
@@ -2551,6 +2576,8 @@ private final class AgentRuntime: NSObject, NSApplicationDelegate {
     }
 
     func applicationWillTerminate(_ notification: Notification) {
+        unclaimedSessionTimeout?.cancel()
+        unclaimedSessionTimeout = nil
         listener?.stop()
     }
 }
@@ -3456,14 +3483,25 @@ private final class ButtonTarget: NSObject {
 private final class SocketListener: @unchecked Sendable {
     private let socketPath: String
     private let token: String?
+    private let onSessionClaimed: () -> Void
+    private let onSessionClosed: () -> Void
     private let provider = Provider()
     private let providerLock = NSLock()
+    private let sessionLock = NSLock()
+    private var sessionOwnership = AgentSessionOwnership()
     private var socketFd: Int32 = -1
     private var isStopped = false
 
-    init(socketPath: String, token: String?) throws {
+    init(
+        socketPath: String,
+        token: String?,
+        onSessionClaimed: @escaping () -> Void,
+        onSessionClosed: @escaping () -> Void
+    ) throws {
         self.socketPath = socketPath
         self.token = token
+        self.onSessionClaimed = onSessionClaimed
+        self.onSessionClosed = onSessionClosed
         try bindSocket()
     }
 
@@ -3545,7 +3583,15 @@ private final class SocketListener: @unchecked Sendable {
     }
 
     private func handleConnection(_ fd: Int32) {
-        defer { close(fd) }
+        defer {
+            sessionLock.lock()
+            let shouldTerminate = sessionOwnership.disconnect(fd)
+            sessionLock.unlock()
+            close(fd)
+            if shouldTerminate {
+                onSessionClosed()
+            }
+        }
         let authorizedPeer = peerProcessId(fd).map(isAuthorizedAgentPeer) == true
         let decoder = JSONDecoder()
         while let line = readLine(from: fd) {
@@ -3554,6 +3600,15 @@ private final class SocketListener: @unchecked Sendable {
             else {
                 continue
             }
+            sessionLock.lock()
+            let claimed = sessionOwnership.registerConnection(
+                fd,
+                authenticated: isAuthenticated(request: request, authorizedPeer: authorizedPeer)
+            )
+            sessionLock.unlock()
+            if claimed {
+                onSessionClaimed()
+            }
             let response = handleRequest(
                 provider: provider,
                 lock: providerLock,
@@ -3564,6 +3619,11 @@ private final class SocketListener: @unchecked Sendable {
             writeJSON(response, to: fd)
         }
     }
+
+    private func isAuthenticated(request: Request, authorizedPeer: Bool) -> Bool {
+        guard let token else { return true }
+        return request.token == token && authorizedPeer
+    }
 }
 
 private func existingPathMode(_ path: String) -> mode_t? {
diff --git a/native/computer-use-macos/Sources/OrcaComputerUseMacOSCore/AgentSessionOwnership.swift b/native/computer-use-macos/Sources/OrcaComputerUseMacOSCore/AgentSessionOwnership.swift
new file mode 100644
index 00000000000..0fb5258163a
--- /dev/null
+++ b/native/computer-use-macos/Sources/OrcaComputerUseMacOSCore/AgentSessionOwnership.swift
@@ -0,0 +1,19 @@
+public struct AgentSessionOwnership: Sendable {
+    private var authenticatedConnections: Set<Int32> = []
+    private var wasClaimed = false
+
+    public init() {}
+
+    public mutating func registerConnection(_ connection: Int32, authenticated: Bool) -> Bool {
+        guard authenticated else { return false }
+        let inserted = authenticatedConnections.insert(connection).inserted
+        guard inserted, !wasClaimed else { return false }
+        wasClaimed = true
+        return true
+    }
+
+    public mutating func disconnect(_ connection: Int32) -> Bool {
+        guard authenticatedConnections.remove(connection) != nil else { return false }
+        return wasClaimed && authenticatedConnections.isEmpty
+    }
+}
diff --git a/native/computer-use-macos/Tests/OrcaComputerUseMacOSTests/AgentSessionOwnershipTests.swift b/native/computer-use-macos/Tests/OrcaComputerUseMacOSTests/AgentSessionOwnershipTests.swift
new file mode 100644
index 00000000000..f050ac5a5e4
--- /dev/null
+++ b/native/computer-use-macos/Tests/OrcaComputerUseMacOSTests/AgentSessionOwnershipTests.swift
@@ -0,0 +1,41 @@
+import OrcaComputerUseMacOSCore
+import XCTest
+
+final class AgentSessionOwnershipTests: XCTestCase {
+    func testUnclaimedDisconnectDoesNotTerminateAgent() {
+        var ownership = AgentSessionOwnership()
+
+        XCTAssertFalse(ownership.disconnect(12))
+    }
+
+    func testUnauthenticatedConnectionCannotClaimOrRetainAgent() {
+        var ownership = AgentSessionOwnership()
+
+        XCTAssertFalse(ownership.registerConnection(12, authenticated: false))
+        XCTAssertFalse(ownership.disconnect(12))
+    }
+
+    func testLastAuthenticatedDisconnectTerminatesAgent() {
+        var ownership = AgentSessionOwnership()
+
+        XCTAssertTrue(ownership.registerConnection(12, authenticated: true))
+        XCTAssertTrue(ownership.disconnect(12))
+    }
+
+    func testAgentWaitsForEveryAuthenticatedConnectionToClose() {
+        var ownership = AgentSessionOwnership()
+
+        XCTAssertTrue(ownership.registerConnection(12, authenticated: true))
+        XCTAssertFalse(ownership.registerConnection(13, authenticated: true))
+        XCTAssertFalse(ownership.disconnect(12))
+        XCTAssertTrue(ownership.disconnect(13))
+    }
+
+    func testDuplicateRegistrationDoesNotRetainAgent() {
+        var ownership = AgentSessionOwnership()
+
+        XCTAssertTrue(ownership.registerConnection(12, authenticated: true))
+        XCTAssertFalse(ownership.registerConnection(12, authenticated: true))
+        XCTAssertTrue(ownership.disconnect(12))
+    }
+}