diff --git a/doc/api/fs.md b/doc/api/fs.md
index ff52cfa5a36e21..ebef4e264fea69 100644
--- a/doc/api/fs.md
+++ b/doc/api/fs.md
@@ -476,11 +476,14 @@ Reads data from the file and stores that in the given buffer.
 If the file is not modified concurrently, the end-of-file is reached when the
 number of bytes read is zero.
 
-#### `filehandle.readableWebStream()`
+#### `filehandle.readableWebStream([options])`
 
 <!-- YAML
 added: v17.0.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/58548
+    description: Added the `autoClose` option.
   - version: v24.0.0
     pr-url: https://github.com/nodejs/node/pull/57513
     description: Marking the API stable.
@@ -496,6 +499,9 @@ changes:
     description: Added option to create a 'bytes' stream.
 -->
 
+* `options` {Object}
+  * `autoClose` {boolean} When true, causes the {FileHandle} to be closed when the
+    stream is closed. **Default:** `false`
 * Returns: {ReadableStream}
 
 Returns a byte-oriented `ReadableStream` that may be used to read the file's
diff --git a/lib/internal/fs/promises.js b/lib/internal/fs/promises.js
index eff9769f90728a..a5607810ca5bb2 100644
--- a/lib/internal/fs/promises.js
+++ b/lib/internal/fs/promises.js
@@ -86,7 +86,6 @@ const {
   validateInteger,
   validateObject,
   validateOneOf,
-  validateString,
   kValidateObjectAllowNullable,
 } = require('internal/validators');
 const pathModule = require('path');
@@ -279,9 +278,10 @@ class FileHandle extends EventEmitter {
   /**
    * @typedef {import('../webstreams/readablestream').ReadableStream
    * } ReadableStream
+   * @param {{ type?: 'bytes', autoClose?: boolean }} [options]
    * @returns {ReadableStream}
    */
-  readableWebStream(options = { __proto__: null, type: 'bytes' }) {
+  readableWebStream(options = kEmptyObject) {
     if (this[kFd] === -1)
       throw new ERR_INVALID_STATE('The FileHandle is closed');
     if (this[kClosePromise])
@@ -290,10 +290,15 @@ class FileHandle extends EventEmitter {
       throw new ERR_INVALID_STATE('The FileHandle is locked');
     this[kLocked] = true;
 
-    if (options.type !== undefined) {
-      validateString(options.type, 'options.type');
-    }
-    if (options.type !== 'bytes') {
+    validateObject(options, 'options');
+    const {
+      type = 'bytes',
+      autoClose = false,
+    } = options;
+
+    validateBoolean(autoClose, 'options.autoClose');
+
+    if (type !== 'bytes') {
       process.emitWarning(
         'A non-"bytes" options.type has no effect. A byte-oriented steam is ' +
         'always created.',
@@ -301,9 +306,11 @@ class FileHandle extends EventEmitter {
       );
     }
 
-
     const readFn = FunctionPrototypeBind(this.read, this);
-    const ondone = FunctionPrototypeBind(this[kUnref], this);
+    const ondone = async () => {
+      this[kUnref]();
+      if (autoClose) await this.close();
+    };
 
     const ReadableStream = lazyReadableStream();
     const readable = new ReadableStream({
@@ -315,15 +322,15 @@ class FileHandle extends EventEmitter {
         const { bytesRead } = await readFn(view, view.byteOffset, view.byteLength);
 
         if (bytesRead === 0) {
-          ondone();
           controller.close();
+          await ondone();
         }
 
         controller.byobRequest.respond(bytesRead);
       },
 
-      cancel() {
-        ondone();
+      async cancel() {
+        await ondone();
       },
     });
 
diff --git a/test/es-module/test-wasm-web-api.js b/test/es-module/test-wasm-web-api.js
index b199393a18c370..879748e4403b07 100644
--- a/test/es-module/test-wasm-web-api.js
+++ b/test/es-module/test-wasm-web-api.js
@@ -106,7 +106,9 @@ function testCompileStreamingRejectionUsingFetch(responseCallback, rejection) {
   // Response whose body is a ReadableStream instead of calling fetch().
   await testCompileStreamingSuccess(async () => {
     const handle = await fs.open(fixtures.path('simple.wasm'));
-    const stream = handle.readableWebStream();
+    // We set the autoClose option to true so that the file handle is closed
+    // automatically when the stream is completed or canceled.
+    const stream = handle.readableWebStream({ autoClose: true });
     return Promise.resolve(new Response(stream, {
       status: 200,
       headers: { 'Content-Type': 'application/wasm' }
diff --git a/test/parallel/test-filehandle-autoclose.mjs b/test/parallel/test-filehandle-autoclose.mjs
new file mode 100644
index 00000000000000..11497c6ac2ec9a
--- /dev/null
+++ b/test/parallel/test-filehandle-autoclose.mjs
@@ -0,0 +1,30 @@
+import '../common/index.mjs';
+import { open } from 'node:fs/promises';
+import { rejects } from 'node:assert';
+
+{
+  const fh = await open(new URL(import.meta.url));
+
+  // TODO: remove autoClose option when it becomes default
+  const readableStream = fh.readableWebStream({ autoClose: true });
+
+  // Consume the stream
+  await new Response(readableStream).text();
+
+  // If reading the FileHandle after the stream is consumed fails,
+  // then we assume the autoClose option worked as expected.
+  await rejects(fh.read(), { code: 'EBADF' });
+}
+
+{
+  await using fh = await open(new URL(import.meta.url));
+
+  const readableStream = fh.readableWebStream({ autoClose: false });
+
+  // Consume the stream
+  await new Response(readableStream).text();
+
+  // Filehandle must be still open
+  await fh.read();
+  await fh.close();
+}