diff --git a/packages/rest/__tests__/RequestHandler.test.ts b/packages/rest/__tests__/RequestHandler.test.ts
index e3333dfb5..b1d388304 100644
--- a/packages/rest/__tests__/RequestHandler.test.ts
+++ b/packages/rest/__tests__/RequestHandler.test.ts
@@ -1,5 +1,6 @@
 /* eslint-disable id-length */
 /* eslint-disable promise/prefer-await-to-then */
+import { getEventListeners } from 'node:events';
 import { MockAgent, setGlobalDispatcher } from 'undici';
 import type { Interceptable, MockInterceptor } from 'undici/types/mock-interceptor.js';
 import { beforeEach, afterEach, test, expect, vitest } from 'vitest';
@@ -549,6 +550,22 @@ test('malformedRequest', async () => {
 	await expect(api.get('/malformedRequest')).rejects.toBeInstanceOf(DiscordAPIError);
 });
 
+test('remove abort listeners after requests complete', async () => {
+	mockPool
+		.intercept({
+			path: genPath('/abort-listener-cleanup'),
+			method: 'GET',
+		})
+		.reply(200, { message: 'Hello World' }, responseOptions)
+		.times(2);
+
+	const controller = new AbortController();
+	for (let index = 0; index < 2; index++) {
+		await api.get('/abort-listener-cleanup', { signal: controller.signal });
+		expect(getEventListeners(controller.signal, 'abort')).toHaveLength(0);
+	}
+});
+
 // TODO: flaky due to changes in undici
 test.skip('abort', async () => {
 	mockPool
diff --git a/packages/rest/src/lib/handlers/Shared.ts b/packages/rest/src/lib/handlers/Shared.ts
index 05600f9be..8ea37a55a 100644
--- a/packages/rest/src/lib/handlers/Shared.ts
+++ b/packages/rest/src/lib/handlers/Shared.ts
@@ -71,12 +71,17 @@ export async function makeNetworkRequest(
 		() => controller.abort(),
 		normalizeTimeout(manager.options.timeout, routeId.bucketRoute, requestData.body),
 	);
-	if (requestData.signal) {
+	const userSignal = requestData.signal;
+	let onUserAbort: (() => void) | undefined;
+	if (userSignal) {
 		// If the user signal was aborted, abort the controller, else abort the local signal.
 		// The reason why we don't re-use the user's signal, is because users may use the same signal for multiple
 		// requests, and we do not want to cause unexpected side-effects.
-		if (requestData.signal.aborted) controller.abort();
-		else requestData.signal.addEventListener('abort', () => controller.abort());
+		if (userSignal.aborted) controller.abort();
+		else {
+			onUserAbort = () => controller.abort();
+			userSignal.addEventListener('abort', onUserAbort);
+		}
 	}
 
 	let res: ResponseLike;
@@ -108,6 +113,7 @@ export async function makeNetworkRequest(
 		throw error;
 	} finally {
 		clearTimeout(timeout);
+		if (onUserAbort) userSignal!.removeEventListener('abort', onUserAbort);
 	}
 
 	if (manager.listenerCount(RESTEvents.Response)) {