diff --git a/src/cli/daemon-cli/lifecycle.test.ts b/src/cli/daemon-cli/lifecycle.test.ts
index 53ded2b5790..20ee6a69a76 100644
--- a/src/cli/daemon-cli/lifecycle.test.ts
+++ b/src/cli/daemon-cli/lifecycle.test.ts
@@ -326,6 +326,14 @@ describe("runDaemonRestart health checks", () => {
     expect(signalVerifiedGatewayPidSync).toHaveBeenCalledWith(4300, "SIGTERM");
   });
 
+  it("skips gateway port resolution on stop when the service manager handles the stop", async () => {
+    await runDaemonStop({ json: true });
+
+    expect(service.readCommand).not.toHaveBeenCalled();
+    expect(loadConfig).not.toHaveBeenCalled();
+    expect(resolveGatewayPort).not.toHaveBeenCalled();
+  });
+
   it("signals a single unmanaged gateway process on restart", async () => {
     findVerifiedGatewayListenerPidsOnPortSync.mockReturnValue([4200]);
     mockUnmanagedRestart({ runPostRestartCheck: true });
diff --git a/src/cli/daemon-cli/lifecycle.ts b/src/cli/daemon-cli/lifecycle.ts
index 540d38c2a55..306c1d73ce1 100644
--- a/src/cli/daemon-cli/lifecycle.ts
+++ b/src/cli/daemon-cli/lifecycle.ts
@@ -157,14 +157,17 @@ export async function runDaemonStart(opts: DaemonLifecycleOptions = {}) {
 
 export async function runDaemonStop(opts: DaemonLifecycleOptions = {}) {
   const service = resolveGatewayService();
-  const gatewayPort = await resolveGatewayLifecyclePort(service).catch(() =>
-    resolveGatewayPortFallback(),
-  );
+  let gatewayPortPromise: Promise<number> | undefined;
   return await runServiceStop({
     serviceNoun: "Gateway",
     service,
     opts,
-    onNotLoaded: async () => stopGatewayWithoutServiceManager(gatewayPort),
+    onNotLoaded: async () => {
+      gatewayPortPromise ??= resolveGatewayLifecyclePort(service).catch(() =>
+        resolveGatewayPortFallback(),
+      );
+      return await stopGatewayWithoutServiceManager(await gatewayPortPromise);
+    },
   });
 }