diff --git a/lib/internal/vfs/file_handle.js b/lib/internal/vfs/file_handle.js
index 4d28abde535e..adf6332941ec 100644
--- a/lib/internal/vfs/file_handle.js
+++ b/lib/internal/vfs/file_handle.js
@@ -429,6 +429,7 @@ class MemoryFileHandle extends VirtualFileHandle {
   #size;
   #entry;
   #getStats;
+  #published; // The entry content this handle last saw or wrote.
 
   #checkClosed(syscall) {
     if (this.closed) {
@@ -450,6 +451,7 @@ class MemoryFileHandle extends VirtualFileHandle {
     this.#size = content.length;
     this.#entry = entry;
     this.#getStats = getStats;
+    this.#published = content;
 
     // O_TRUNC empties the file at open time. O_APPEND does not move the
     // read offset: it only forces writes to the end, so the position stays
@@ -459,10 +461,24 @@ class MemoryFileHandle extends VirtualFileHandle {
       this.#size = 0;
       if (entry) {
         entry.content = this.#content;
+        this.#published = this.#content;
       }
     }
   }
 
+  /**
+   * Adopts the entry's content if another handle replaced it, since an
+   * open descriptor is a live view of the file, not a snapshot.
+   */
+  #sync() {
+    const entry = this.#entry;
+    if (entry && entry.content !== this.#published) {
+      this.#content = entry.content;
+      this.#size = entry.content.length;
+      this.#published = entry.content;
+    }
+  }
+
   /**
    * Throws EBADF if the handle was not opened for writing.
    */
@@ -499,6 +515,7 @@ class MemoryFileHandle extends VirtualFileHandle {
     if (this.#entry?.isDynamic && this.#entry.isDynamic()) {
       return this.#entry.getContentSync();
     }
+    this.#sync();
     return this.#content.subarray(0, this.#size);
   }
 
@@ -572,6 +589,7 @@ class MemoryFileHandle extends VirtualFileHandle {
   writeSync(buffer, offset, length, position) {
     this.#checkClosed('write');
     this.#checkWritable();
+    this.#sync();
 
     // In append mode, always write at the end
     const useCurrentPosition = isCurrentPosition(position);
@@ -603,6 +621,7 @@ class MemoryFileHandle extends VirtualFileHandle {
       this.#entry.content = this.#content.subarray(0, this.#size);
       this.#entry.mtime = now;
       this.#entry.ctime = now;
+      this.#published = this.#entry.content;
     }
 
     // Update position if not using explicit position
@@ -693,6 +712,7 @@ class MemoryFileHandle extends VirtualFileHandle {
   statSync(options) {
     this.#checkClosed('fstat');
     if (this.#getStats) {
+      this.#sync();
       return this.#getStats(this.#size);
     }
     throw new ERR_INVALID_STATE('stats not available');
@@ -741,6 +761,7 @@ class MemoryFileHandle extends VirtualFileHandle {
   truncateSync(len = 0) {
     this.#checkClosed('ftruncate');
     this.#checkWritable();
+    this.#sync();
 
     if (len < this.#size) {
       // Zero out truncated region to avoid stale data
@@ -764,6 +785,7 @@ class MemoryFileHandle extends VirtualFileHandle {
       this.#entry.content = this.#content.subarray(0, this.#size);
       this.#entry.mtime = now;
       this.#entry.ctime = now;
+      this.#published = this.#entry.content;
     }
   }
 
diff --git a/test/parallel/test-vfs-memory-handle-live-view.js b/test/parallel/test-vfs-memory-handle-live-view.js
new file mode 100644
index 000000000000..58a9ce321102
--- /dev/null
+++ b/test/parallel/test-vfs-memory-handle-live-view.js
@@ -0,0 +1,94 @@
+// Flags: --experimental-vfs
+'use strict';
+// MemoryProvider: an open handle is a live view of the file, not a snapshot
+// taken at open time. Writes made through the provider or through another
+// handle must be visible to handles that are already open, as they are on a
+// real filesystem. Refs: https://github.com/nodejs/node/issues/66355
+const common = require('../common');
+const assert = require('assert');
+const { create } = require('node:vfs');
+
+// Content replaced through the provider is seen by an open read handle.
+{
+  const { provider: p } = create();
+  p.writeFileSync('/f', 'AAAA');
+  const h = p.openSync('/f', 'r');
+  p.writeFileSync('/f', '0123456789');
+
+  const b = Buffer.alloc(10);
+  assert.strictEqual(h.readSync(b, 0, 10, 0), 10);
+  assert.strictEqual(b.toString(), '0123456789');
+  assert.strictEqual(h.readFileSync('utf8'), '0123456789');
+  assert.strictEqual(h.statSync().size, 10);
+  assert.strictEqual(p.statSync('/f').size, 10);
+  h.readFile('utf8').then(common.mustCall((s) => {
+    assert.strictEqual(s, '0123456789');
+    h.closeSync();
+  }));
+}
+
+// A shrinking rewrite is seen too: reads stop at the new end.
+{
+  const { provider: p } = create();
+  p.writeFileSync('/f', '0123456789');
+  const h = p.openSync('/f', 'r');
+  p.writeFileSync('/f', 'AB');
+
+  const b = Buffer.alloc(10);
+  assert.strictEqual(h.readSync(b, 0, 10, 0), 2);
+  assert.strictEqual(b.subarray(0, 2).toString(), 'AB');
+  assert.strictEqual(h.readFileSync('utf8'), 'AB');
+  assert.strictEqual(h.statSync().size, 2);
+  h.closeSync();
+}
+
+// Two writable handles on the same file do not clobber each other.
+{
+  const { provider: p } = create();
+  p.writeFileSync('/f', 'AAAA');
+  const h1 = p.openSync('/f', 'r+');
+  const h2 = p.openSync('/f', 'r+');
+
+  h1.writeSync(Buffer.from('XY'), 0, 2, 0);
+  h2.writeSync(Buffer.from('Z'), 0, 1, 3);
+  assert.strictEqual(p.readFileSync('/f', 'utf8'), 'XYAZ');
+  assert.strictEqual(h1.readFileSync('utf8'), 'XYAZ');
+
+  // Growing through one handle is visible to the other.
+  h1.writeSync(Buffer.from('0123456789'), 0, 10, 4);
+  assert.strictEqual(h2.statSync().size, 14);
+  assert.strictEqual(h2.readFileSync('utf8'), 'XYAZ0123456789');
+
+  // Truncating through one handle is visible to the other.
+  h2.truncateSync(3);
+  assert.strictEqual(h1.statSync().size, 3);
+  assert.strictEqual(h1.readFileSync('utf8'), 'XYA');
+
+  h1.closeSync();
+  h2.closeSync();
+}
+
+// A write through a handle opened before the file was replaced lands in the
+// current content instead of resurrecting the old bytes.
+{
+  const { provider: p } = create();
+  p.writeFileSync('/f', 'AAAA');
+  const h = p.openSync('/f', 'r+');
+  p.writeFileSync('/f', 'BB');
+
+  h.writeSync(Buffer.from('C'), 0, 1, 3);
+  assert.deepStrictEqual(p.readFileSync('/f'), Buffer.from('BB\0C', 'latin1'));
+  h.closeSync();
+}
+
+// An append handle opened earlier appends after the current end.
+{
+  const { provider: p } = create();
+  p.writeFileSync('/f', 'AAAA');
+  const h = p.openSync('/f', 'a');
+  p.writeFileSync('/f', 'B');
+
+  h.writeSync(Buffer.from('C'), 0, 1, null);
+  assert.strictEqual(p.readFileSync('/f', 'utf8'), 'BC');
+  h.closeSync();
+}