diff --git a/lib/web/fetch/request.js b/lib/web/fetch/request.js
index 66f8150cb82..2c3252bb6a5 100644
--- a/lib/web/fetch/request.js
+++ b/lib/web/fetch/request.js
@@ -30,8 +30,12 @@ const { getMaxListeners, setMaxListeners, defaultMaxListeners } = require('node:
 
 const kAbortController = Symbol('abortController')
 
-const requestFinalizer = new FinalizationRegistry(({ signal, abort }) => {
-  signal.removeEventListener('abort', abort)
+// The held value must not keep the caller's signal alive: if anything reachable
+// from that signal can reach the Request, it would also keep the registry's
+// target (the Request's AbortController) alive, and neither would ever be
+// collected. A signal that is already gone has no listener left to remove.
+const requestFinalizer = new FinalizationRegistry(({ signalRef, abort }) => {
+  signalRef.deref()?.removeEventListener('abort', abort)
 })
 
 const dependentControllerMap = new WeakMap()
@@ -449,7 +453,7 @@ class Request {
         // Without it, you cannot unregister.
         // https://developer.mozilla.org/en-US/docs/Web/JavaScript/Reference/Global_Objects/FinalizationRegistry
         // abort is used as the unregister key. (because it is unique)
-        requestFinalizer.register(ac, { signal, abort }, abort)
+        requestFinalizer.register(ac, { signalRef: new WeakRef(signal), abort }, abort)
 
         // Allow the listener to be removed deterministically once the fetch
         // that owns this request has settled, instead of relying solely on the
diff --git a/test/fetch/request-signal-cycle.js b/test/fetch/request-signal-cycle.js
new file mode 100644
index 00000000000..c6fb4fd65db
--- /dev/null
+++ b/test/fetch/request-signal-cycle.js
@@ -0,0 +1,100 @@
+'use strict'
+
+const { test } = require('node:test')
+const assert = require('node:assert')
+const { setImmediate: tick } = require('node:timers/promises')
+const { Request } = require('../..')
+
+const hasGC = typeof global.gc !== 'undefined'
+
+// A Request that follows a caller's signal is registered in a
+// FinalizationRegistry keyed on its own AbortController. The held value used to
+// keep a strong reference to the caller's signal. When anything reachable from
+// that signal could reach the Request (a listener or a property closing over
+// it), the held value kept the registry's own target alive, so neither the
+// Request nor anything it held was ever collected.
+async function collected (ref) {
+  for (let i = 0; i < 10 && ref.deref() !== undefined; i++) {
+    await tick()
+    global.gc()
+  }
+  return ref.deref() === undefined
+}
+
+test('a Request is collected when a listener on its signal references it', async () => {
+  if (!hasGC) {
+    throw new Error('gc is not available. Run with \'--expose-gc\'.')
+  }
+
+  let ref
+  ;(() => {
+    const controller = new AbortController()
+    const request = new Request('http://localhost', { signal: controller.signal })
+    controller.signal.addEventListener('abort', () => request.url)
+    ref = new WeakRef(request)
+  })()
+
+  assert.ok(await collected(ref))
+})
+
+test('a Request is collected when a property of its signal references it', async () => {
+  if (!hasGC) {
+    throw new Error('gc is not available. Run with \'--expose-gc\'.')
+  }
+
+  let ref
+  ;(() => {
+    const controller = new AbortController()
+    const request = new Request('http://localhost', { signal: controller.signal })
+    controller.signal.cleanup = () => request.url
+    ref = new WeakRef(request)
+  })()
+
+  assert.ok(await collected(ref))
+})
+
+test('the abort listener is still removed when the Request is collected', async () => {
+  if (!hasGC) {
+    throw new Error('gc is not available. Run with \'--expose-gc\'.')
+  }
+
+  const { getEventListeners } = require('node:events')
+  const controller = new AbortController()
+  let ref
+  ;(() => {
+    const request = new Request('http://localhost', { signal: controller.signal })
+    ref = new WeakRef(request)
+  })()
+
+  assert.ok(await collected(ref))
+  // The registry's cleanup callback runs after the collection, on its own task.
+  for (let i = 0; i < 10 && getEventListeners(controller.signal, 'abort').length > 0; i++) {
+    await tick()
+    global.gc()
+  }
+  assert.strictEqual(getEventListeners(controller.signal, 'abort').length, 0)
+})
+
+test('a timeout signal nobody else references still aborts the Request', { timeout: 5000 }, async () => {
+  if (!hasGC) {
+    throw new Error('gc is not available. Run with \'--expose-gc\'.')
+  }
+
+  // The held value no longer keeps the signal alive, so this relies on the
+  // signal keeping itself alive while it has an abort listener and can still fire.
+  const request = new Request('http://localhost', { signal: AbortSignal.timeout(100) })
+  const aborted = new Promise((resolve) => request.signal.addEventListener('abort', resolve, { once: true }))
+  for (let i = 0; i < 10; i++) {
+    await tick()
+    global.gc()
+  }
+
+  // The timeout's own timer is unref'd and would let the process exit first.
+  const keepAlive = setInterval(() => {}, 1000)
+  try {
+    await aborted
+  } finally {
+    clearInterval(keepAlive)
+  }
+  assert.strictEqual(request.signal.aborted, true)
+})