diff --git a/engine/packages/guard-core/src/utils.rs b/engine/packages/guard-core/src/utils.rs
index d6afd21e87..97e4c95786 100644
--- a/engine/packages/guard-core/src/utils.rs
+++ b/engine/packages/guard-core/src/utils.rs
@@ -487,7 +487,6 @@ fn is_retryable_guard_http_error(code: &str) -> bool {
 			| "tunnel_request_aborted"
 			| "tunnel_message_timeout"
 			| "tunnel_response_closed"
-			| "gateway_response_start_timeout"
 	)
 }
 
diff --git a/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/gateway-response-start-timeout.ts b/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/gateway-response-start-timeout.ts
new file mode 100644
index 0000000000..b7689710ac
--- /dev/null
+++ b/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/gateway-response-start-timeout.ts
@@ -0,0 +1,23 @@
+import { actor } from "rivetkit";
+
+export const responseStartTimeoutActor = actor({
+	state: { runs: 0 },
+	createVars: () => ({ waiting: [] as Array<() => void> }),
+	actions: {
+		// Only the first run waits for `release`, so a duplicate run reaches the
+		// caller as a result instead of a timeout.
+		waitForRelease: async (c) => {
+			c.state.runs += 1;
+			if (c.state.runs === 1) {
+				await new Promise<void>((resolve) =>
+					c.vars.waiting.push(resolve),
+				);
+			}
+			return c.state.runs;
+		},
+		release: (c) => {
+			for (const resolve of c.vars.waiting.splice(0)) resolve();
+		},
+		runs: (c) => c.state.runs,
+	},
+});
diff --git a/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/registry-static.ts b/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/registry-static.ts
index ac165dd402..58a3381df9 100644
--- a/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/registry-static.ts
+++ b/rivetkit-typescript/packages/rivetkit/fixtures/driver-test-suite/registry-static.ts
@@ -62,6 +62,7 @@ import {
 } from "./destroy";
 import { customTimeoutActor, errorHandlingActor } from "./error-handling";
 import { fileSystemHibernationCleanupActor } from "./file-system-hibernation-cleanup";
+import { responseStartTimeoutActor } from "./gateway-response-start-timeout";
 import { hibernationActor, hibernationSleepWindowActor } from "./hibernation";
 import { kvActor } from "./kv";
 import { largePayloadActor, largePayloadConnActor } from "./large-payloads";
@@ -276,6 +277,8 @@ export const registry = setup({
 		manyQueueRunParentActor,
 		// From action-inputs.ts
 		inputActor,
+		// From gateway-response-start-timeout.ts
+		responseStartTimeoutActor,
 		// From action-timeout.ts
 		shortTimeoutActor,
 		longTimeoutActor,
diff --git a/rivetkit-typescript/packages/rivetkit/src/client/lifecycle-errors.ts b/rivetkit-typescript/packages/rivetkit/src/client/lifecycle-errors.ts
index 4466aa3e01..0f726914ef 100644
--- a/rivetkit-typescript/packages/rivetkit/src/client/lifecycle-errors.ts
+++ b/rivetkit-typescript/packages/rivetkit/src/client/lifecycle-errors.ts
@@ -166,8 +166,7 @@ function isRetryableGuardGatewayHttpError(code: string): boolean {
 		code === "actor_stopped_while_waiting" ||
 		code === "tunnel_request_aborted" ||
 		code === "tunnel_message_timeout" ||
-		code === "tunnel_response_closed" ||
-		code === "gateway_response_start_timeout"
+		code === "tunnel_response_closed"
 	);
 }
 
diff --git a/rivetkit-typescript/packages/rivetkit/tests/driver/gateway-response-start-timeout.test.ts b/rivetkit-typescript/packages/rivetkit/tests/driver/gateway-response-start-timeout.test.ts
new file mode 100644
index 0000000000..f1d32f1590
--- /dev/null
+++ b/rivetkit-typescript/packages/rivetkit/tests/driver/gateway-response-start-timeout.test.ts
@@ -0,0 +1,32 @@
+import { describe, expect, test } from "vitest";
+import { describeDriverMatrix } from "./shared-matrix";
+import { setupDriverTest } from "./shared-utils";
+
+describeDriverMatrix(
+	"Gateway Response Start Timeout",
+	(driverTestConfig) => {
+		describe("gateway response start timeout", () => {
+			test("an action that outlives the timeout runs once, and the caller gets the timeout", async (c) => {
+				const { client } = await setupDriverTest(c, driverTestConfig);
+				const actor = client.responseStartTimeoutActor.getOrCreate([
+					"runs-once",
+				]);
+
+				// The action reached the actor, so its result is unknown and
+				// neither the gateway nor the client may send it again.
+				await expect(actor.waitForRelease()).rejects.toMatchObject({
+					group: "guard",
+					code: "gateway_response_start_timeout",
+				});
+				await actor.release();
+				expect(await actor.runs()).toBe(1);
+			});
+		});
+	},
+	{
+		runtimes: ["native"],
+		encodings: ["bare"],
+		sqliteBackends: ["remote"],
+		config: { engine: { gatewayResponseStartTimeoutMs: 2_000 } },
+	},
+);
diff --git a/rivetkit-typescript/packages/rivetkit/tests/lifecycle-errors.test.ts b/rivetkit-typescript/packages/rivetkit/tests/lifecycle-errors.test.ts
index 6d8b4c80de..b6ef15452a 100644
--- a/rivetkit-typescript/packages/rivetkit/tests/lifecycle-errors.test.ts
+++ b/rivetkit-typescript/packages/rivetkit/tests/lifecycle-errors.test.ts
@@ -10,7 +10,6 @@ describe("lifecycle error retry classification", () => {
 		"tunnel_request_aborted",
 		"tunnel_message_timeout",
 		"tunnel_response_closed",
-		"gateway_response_start_timeout",
 	])("classifies guard.%s as retryable", (code) => {
 		expect(
 			isRetryableLifecycleRequestError(
diff --git a/rivetkit-typescript/packages/rivetkit/tests/shared-engine.ts b/rivetkit-typescript/packages/rivetkit/tests/shared-engine.ts
index b817c8abf5..ccad534a9b 100644
--- a/rivetkit-typescript/packages/rivetkit/tests/shared-engine.ts
+++ b/rivetkit-typescript/packages/rivetkit/tests/shared-engine.ts
@@ -40,6 +40,7 @@ export interface SharedTestEngine {
 
 export interface SharedTestEngineOptions {
 	gateway3?: boolean;
+	gatewayResponseStartTimeoutMs?: number;
 }
 
 interface SharedEngineFiles {
@@ -57,7 +58,10 @@ let sharedEngineProfile: string | undefined;
 let sharedEngineFiles: SharedEngineFiles | undefined;
 
 function resolveSharedEngineProfile(options: SharedTestEngineOptions): string {
-	return JSON.stringify({ gateway3: options.gateway3 ?? false });
+	return JSON.stringify({
+		gateway3: options.gateway3 ?? false,
+		gatewayResponseStartTimeoutMs: options.gatewayResponseStartTimeoutMs,
+	});
 }
 
 function resolveSharedEngineFiles(profile: string): SharedEngineFiles {
@@ -289,13 +293,19 @@ async function spawnSharedEngine(
 					},
 				},
 			},
-			pegboard: options.gateway3
-				? {
-						gateway_update_ping_interval_ms: 250,
-						gateway_tunnel_ping_timeout_ms: 2_000,
-						gateway_response_start_timeout_ms: 3_000,
-					}
-				: undefined,
+			// JSON.stringify drops undefined fields, and an empty pegboard
+			// section is the same as none.
+			pegboard: {
+				...(options.gateway3
+					? {
+							gateway_update_ping_interval_ms: 250,
+							gateway_tunnel_ping_timeout_ms: 2_000,
+						}
+					: {}),
+				gateway_response_start_timeout_ms:
+					options.gatewayResponseStartTimeoutMs ??
+					(options.gateway3 ? 3_000 : undefined),
+			},
 			features: options.gateway3
 				? {
 						guard_gateway_v3: {