diff --git a/lib/fs.js b/lib/fs.js
index 4436fa2df6e6..c79f57537020 100644
--- a/lib/fs.js
+++ b/lib/fs.js
@@ -3750,6 +3750,12 @@ function mkdtempSync(prefix, options) {
  * @returns {object} A disposable object with a "path" property.
  */
 function mkdtempDisposableSync(prefix, options) {
+  const h = vfsState.handlers;
+  if (h !== null) {
+    const result = h.mkdtempDisposableSync(prefix, options);
+    if (result !== undefined) return result;
+  }
+
   options = getOptions(options);
   if (BufferIsBuffer(prefix)) {
     options = { ...options, encoding: 'buffer' };
diff --git a/lib/internal/fs/promises.js b/lib/internal/fs/promises.js
index c21b1e5740fc..db348476c35e 100644
--- a/lib/internal/fs/promises.js
+++ b/lib/internal/fs/promises.js
@@ -2137,6 +2137,12 @@ async function mkdtemp(prefix, options) {
 }
 
 async function mkdtempDisposable(prefix, options) {
+  const h = vfsState.handlers;
+  if (h !== null) {
+    const promise = h.mkdtempDisposable(prefix, options);
+    if (promise !== undefined) return await promise;
+  }
+
   options = getOptions(options);
   if (BufferIsBuffer(prefix)) {
     options = { ...options, encoding: 'buffer' };
diff --git a/lib/internal/vfs/setup.js b/lib/internal/vfs/setup.js
index a5f1b42659b0..08aeb99dfa2e 100644
--- a/lib/internal/vfs/setup.js
+++ b/lib/internal/vfs/setup.js
@@ -9,6 +9,8 @@ const {
   String,
   StringPrototypeEndsWith,
   StringPrototypeStartsWith,
+  SymbolAsyncDispose,
+  SymbolDispose,
 } = primordials;
 
 const { Buffer } = require('buffer');
@@ -530,6 +532,19 @@ function createVfsHandlers() {
       }
       return result;
     },
+    mkdtempDisposableSync(prefix, options) {
+      return vfsOp(prefix, (vfs, n) => {
+        const dir = vfs.mkdtempSync(n);
+        const remove = () => vfs.rmSync(dir, { recursive: true, force: true });
+        return {
+          path: options?.encoding === 'buffer' ? Buffer.from(dir) : dir,
+          remove,
+          [SymbolDispose]() {
+            remove();
+          },
+        };
+      });
+    },
     opendirSync: (path, options) => vfsOp(path, (vfs, n) => vfs.opendirSync(n, options)),
     openAsBlob(path, options) {
       const pathStr = toPathStr(path);
@@ -860,6 +875,20 @@ function createVfsHandlers() {
       }
       return promise;
     },
+    mkdtempDisposable(prefix, options) {
+      return vfsOp(prefix, async (vfs, n) => {
+        const dir = await vfs.promises.mkdtemp(n);
+        const remove = () => vfs.promises.rm(dir, { recursive: true, force: true });
+        return {
+          __proto__: null,
+          path: options?.encoding === 'buffer' ? Buffer.from(dir) : dir,
+          remove,
+          async [SymbolAsyncDispose]() {
+            await remove();
+          },
+        };
+      });
+    },
     chmod: (path, mode) =>
       vfsOp(path, (vfs, n) => vfs.promises.chmod(n, mode).then(() => true)),
     utimes: (path, atime, mtime) =>
diff --git a/test/parallel/test-vfs-fs-mkdtemp-disposable.js b/test/parallel/test-vfs-fs-mkdtemp-disposable.js
new file mode 100644
index 000000000000..3314f49ce287
--- /dev/null
+++ b/test/parallel/test-vfs-fs-mkdtemp-disposable.js
@@ -0,0 +1,111 @@
+// Flags: --experimental-vfs
+'use strict';
+
+// fs.mkdtempDisposableSync and fs.promises.mkdtempDisposable dispatch to the
+// VFS for a mounted prefix, like mkdtempSync and fs.promises.mkdtemp do, and
+// their remove() deletes the directory from the VFS. A prefix outside the
+// mount still reaches the real file system.
+
+const common = require('../common');
+const assert = require('assert');
+const fs = require('fs');
+const path = require('path');
+const vfs = require('node:vfs');
+const tmpdir = require('../common/tmpdir');
+
+tmpdir.refresh();
+
+const myVfs = vfs.create();
+myVfs.mkdirSync('/work', { recursive: true });
+const mountPoint = myVfs.mount();
+const prefix = path.join(mountPoint, 'work', 'tmp-');
+
+// Sync: created in the VFS, removed from the VFS, removal is idempotent.
+{
+  const result = fs.mkdtempDisposableSync(prefix);
+  assert.ok(result.path.startsWith(prefix));
+  assert.strictEqual(result.path.length, prefix.length + 6);
+  assert.strictEqual(fs.statSync(result.path).isDirectory(), true);
+  assert.deepStrictEqual(fs.readdirSync(path.join(mountPoint, 'work')), [path.basename(result.path)]);
+
+  fs.writeFileSync(path.join(result.path, 'file.txt'), 'data');
+  result.remove();
+  assert.strictEqual(fs.existsSync(result.path), false);
+  assert.deepStrictEqual(fs.readdirSync(path.join(mountPoint, 'work')), []);
+  result.remove();
+}
+
+// Sync: Symbol.dispose
+{
+  const result = fs.mkdtempDisposableSync(prefix);
+  assert.strictEqual(fs.existsSync(result.path), true);
+  result[Symbol.dispose]();
+  assert.strictEqual(fs.existsSync(result.path), false);
+  result[Symbol.dispose]();
+}
+
+// Sync: buffer encoding
+{
+  const result = fs.mkdtempDisposableSync(prefix, { encoding: 'buffer' });
+  assert.ok(Buffer.isBuffer(result.path));
+  assert.ok(result.path.toString().startsWith(prefix));
+  assert.strictEqual(fs.existsSync(result.path), true);
+  result.remove();
+  assert.strictEqual(fs.existsSync(result.path), false);
+}
+
+// Sync: a prefix outside the mount uses the real file system.
+{
+  const result = fs.mkdtempDisposableSync(tmpdir.resolve('real-'));
+  assert.strictEqual(path.dirname(result.path), tmpdir.path);
+  assert.strictEqual(fs.existsSync(result.path), true);
+  result.remove();
+  assert.strictEqual(fs.existsSync(result.path), false);
+}
+
+(async () => {
+  // Promises: created in the VFS, removed from the VFS, removal is idempotent.
+  {
+    const result = await fs.promises.mkdtempDisposable(prefix);
+    assert.ok(result.path.startsWith(prefix));
+    assert.strictEqual(result.path.length, prefix.length + 6);
+    assert.strictEqual(fs.statSync(result.path).isDirectory(), true);
+    assert.deepStrictEqual(fs.readdirSync(path.join(mountPoint, 'work')), [path.basename(result.path)]);
+
+    fs.writeFileSync(path.join(result.path, 'file.txt'), 'data');
+    await result.remove();
+    assert.strictEqual(fs.existsSync(result.path), false);
+    assert.deepStrictEqual(fs.readdirSync(path.join(mountPoint, 'work')), []);
+    await result.remove();
+  }
+
+  // Promises: Symbol.asyncDispose
+  {
+    const result = await fs.promises.mkdtempDisposable(prefix);
+    assert.strictEqual(fs.existsSync(result.path), true);
+    await result[Symbol.asyncDispose]();
+    assert.strictEqual(fs.existsSync(result.path), false);
+    await result[Symbol.asyncDispose]();
+  }
+
+  // Promises: buffer encoding
+  {
+    const result = await fs.promises.mkdtempDisposable(prefix, { encoding: 'buffer' });
+    assert.ok(Buffer.isBuffer(result.path));
+    assert.ok(result.path.toString().startsWith(prefix));
+    assert.strictEqual(fs.existsSync(result.path), true);
+    await result.remove();
+    assert.strictEqual(fs.existsSync(result.path), false);
+  }
+
+  // Promises: a prefix outside the mount uses the real file system.
+  {
+    const result = await fs.promises.mkdtempDisposable(tmpdir.resolve('real-'));
+    assert.strictEqual(path.dirname(result.path), tmpdir.path);
+    assert.strictEqual(fs.existsSync(result.path), true);
+    await result.remove();
+    assert.strictEqual(fs.existsSync(result.path), false);
+  }
+
+  myVfs.unmount();
+})().then(common.mustCall());