diff --git a/src/lib/libsigs.js b/src/lib/libsigs.js
index c5474f4847718..e4e7d0c20ece8 100644
--- a/src/lib/libsigs.js
+++ b/src/lib/libsigs.js
@@ -431,6 +431,7 @@ sigs = {
   _wasmfs_opfs_init_root_directory__sig: 'vp',
   _wasmfs_opfs_insert_directory__sig: 'vpipp',
   _wasmfs_opfs_insert_file__sig: 'vpipp',
+  _wasmfs_opfs_move_dir__sig: 'vpiipp',
   _wasmfs_opfs_move_file__sig: 'vpiipp',
   _wasmfs_opfs_open_access__sig: 'vpip',
   _wasmfs_opfs_open_blob__sig: 'vpip',
diff --git a/src/lib/libwasmfs_opfs.js b/src/lib/libwasmfs_opfs.js
index 4dd7598226298..26ce83f795777 100644
--- a/src/lib/libwasmfs_opfs.js
+++ b/src/lib/libwasmfs_opfs.js
@@ -14,6 +14,69 @@ addToLibrary({
   $wasmfsOPFSBlobs__deps: ["$HandleAllocator"],
   $wasmfsOPFSBlobs: "new HandleAllocator()",
 
+  $wasmOPFSGetParentDir__deps: ['$wasmfsOPFSDirectoryHandles'],
+  $wasmOPFSGetParentDir: async function(handle) {
+    const root = wasmfsOPFSDirectoryHandles.get(1);
+    let fullPath = await root.resolve(handle);
+    if (!fullPath) {
+      throw new Error("Handle not found");
+    }
+    let parent = root;
+    for (let dir of fullPath.slice(0, -1)) {
+      parent = await parent.getDirectoryHandle(dir);
+    }
+    return parent;
+  },
+
+  $wasmOPFSFileMoveWorkaround__deps: ['$wasmOPFSGetParentDir'],
+  $wasmOPFSFileMoveWorkaround: async (fileHandle, newDirHandle, name) => {
+      let newHandle = await newDirHandle.getFileHandle(name, {create: true});
+      let oldParent = await wasmOPFSGetParentDir(fileHandle);
+
+      const fileSize = fileHandle.getSize();
+      const buffer = new Uint8Array(fileSize);
+      let totalRead = 0;
+      while (totalRead < fileSize) {
+        const readBuffer = fileHandle.read(buffer, { at: totalRead });
+        if (readBuffer === 0) {
+          break;
+        }
+        totalRead += readBuffer;
+      }
+      newHandle.truncate(0);
+      await newHandle.write(buffer);
+      newHandle.flush();
+      newHandle.close();
+      fileHandle.close();
+      await oldParent.removeEntry(fileHandle.name);
+  },
+
+  $wasmOPFSDirMoveWorkaround__deps: ['$wasmOPFSGetParentDir'],
+  $wasmOPFSDirMoveWorkaround: async (dirHandle, newDirHandle, name) => {
+    let oldParent = await wasmOPFSGetParentDir(dirHandle);
+    let toDir = await newDirHandle.getDirectoryHandle(name, {create: true});
+    const moveDir = async (fromDir, toDir) => {
+      const entries = await fromDir.entries();
+      let curr;
+      for (curr = await entries.next(); !curr.done; curr = await entries.next() ) {
+        const [name, child] = curr.value;
+        if (child.kind === 'directory') {
+          const newSub = await toDir.getDirectoryHandle(name, {create: true});
+          await moveDir(child, newSub);
+          await fromDir.removeEntry(name);
+        } else {
+          try {
+            await child.move(toDir);
+          } catch {
+            await wasmOPFSFileMoveWorkaround(child, toDir, name);
+          }
+        }
+      }
+    };
+    await moveDir(dirHandle, toDir);
+    await oldParent.removeEntry(dirHandle.name);
+  },
+
 #if !PTHREADS
   // OPFS will only be used on modern browsers that supports JS classes.
   $FileSystemAsyncAccessHandle: class {
@@ -197,7 +260,8 @@ addToLibrary({
 
   _wasmfs_opfs_move_file__deps: ['$wasmfsOPFSFileHandles',
                                  '$wasmfsOPFSDirectoryHandles',
-                                 '$wasmfsOPFSProxyFinish'],
+                                 '$wasmfsOPFSProxyFinish',
+                                 '$wasmOPFSFileMoveWorkaround'],
   _wasmfs_opfs_move_file: async function(ctx, fileID, newParentID, namePtr, errPtr) {
     let name = UTF8ToString(namePtr);
     let fileHandle = wasmfsOPFSFileHandles.get(fileID);
@@ -206,7 +270,43 @@ addToLibrary({
       await fileHandle.move(newDirHandle, name);
     } catch {
       let err = -{{{ cDefs.EIO }}};
-      {{{ makeSetValue('errPtr', 0, 'err', 'i32') }}};
+      try {
+        await wasmOPFSFileMoveWorkaround(fileHandle, newDirHandle, name);
+        wasmfsOPFSFileHandles.allocated[fileID] =
+            await newDirHandle.getFileHandle(name);
+        err = undefined;
+      } catch {
+        // nothing to do, we already set the error above
+      }
+      if (err) {
+        {{{ makeSetValue('errPtr', 0, 'err', 'i32') }}};
+      }
+    }
+    wasmfsOPFSProxyFinish(ctx);
+  },
+
+  _wasmfs_opfs_move_dir__deps: ['$wasmfsOPFSDirectoryHandles',
+    '$wasmfsOPFSProxyFinish',
+    '$wasmOPFSDirMoveWorkaround'],
+
+  _wasmfs_opfs_move_dir: async function(ctx, dirID, newParentID, namePtr, errPtr) {
+    let name = UTF8ToString(namePtr);
+    let dirHandle = wasmfsOPFSDirectoryHandles.get(dirID);
+    let newDirHandle = wasmfsOPFSDirectoryHandles.get(newParentID);
+    try {
+      await dirHandle.move(newDirHandle, name);
+    } catch {
+      let err = -{{{ cDefs.EBUSY }}};
+      try {
+        await wasmOPFSDirMoveWorkaround(dirHandle, newDirHandle, name);
+        wasmfsOPFSDirectoryHandles.allocated[dirID] = await newDirHandle.getDirectoryHandle(name);
+        err = undefined;
+      } catch {
+        // nothing to do, we already set the error above
+      }
+      if (err) {
+        {{{ makeSetValue('errPtr', 0, 'err', 'i32')}}};
+      }
     }
     wasmfsOPFSProxyFinish(ctx);
   },
diff --git a/system/lib/wasmfs/backends/opfs_backend.cpp b/system/lib/wasmfs/backends/opfs_backend.cpp
index 6a5be884cc38b..235f9b0cde6b2 100644
--- a/system/lib/wasmfs/backends/opfs_backend.cpp
+++ b/system/lib/wasmfs/backends/opfs_backend.cpp
@@ -335,10 +335,13 @@ class OPFSDirectory : public Directory {
           ctx.ctx, opfsFile->fileID, dirID, name.c_str(), &err);
       });
     } else {
-      // TODO: Support moving directories once OPFS supports that.
-      // EBUSY can be returned when the directory is "in use by the system,"
-      // which can mean whatever we want.
-      err = -EBUSY;
+      auto opfsDir = std::static_pointer_cast<OPFSDirectory>(file);
+      proxy([&](auto ctx) {
+      _wasmfs_opfs_move_dir(
+        ctx.ctx, opfsDir->dirID, dirID, name.c_str(), &err);
+      });
+      // opfs file handles are all invalid now, so have to clear the cache.
+      opfsDir->locked().removeAllCacheEntries();
     }
     return err;
   }
diff --git a/system/lib/wasmfs/backends/opfs_backend.h b/system/lib/wasmfs/backends/opfs_backend.h
index fc484bdd067b9..507cc24348549 100644
--- a/system/lib/wasmfs/backends/opfs_backend.h
+++ b/system/lib/wasmfs/backends/opfs_backend.h
@@ -39,6 +39,12 @@ void _wasmfs_opfs_move_file(em_proxying_ctx* ctx,
                             const char* name,
                             int* err);
 
+void _wasmfs_opfs_move_dir(em_proxying_ctx* ctx,
+                            int file_id,
+                            int new_parent_id,
+                            const char* name,
+                            int* err);
+
 void _wasmfs_opfs_remove_child(em_proxying_ctx* ctx,
                                int dir_id,
                                const char* name,
diff --git a/system/lib/wasmfs/file.cpp b/system/lib/wasmfs/file.cpp
index c16af931c7228..031c23b5845db 100644
--- a/system/lib/wasmfs/file.cpp
+++ b/system/lib/wasmfs/file.cpp
@@ -134,6 +134,18 @@ Directory::Handle::insertSymlink(const std::string& name,
   return child;
 }
 
+void Directory::Handle::removeAllCacheEntries() {
+  auto& dcache = getDir()->dcache;
+  for (const auto& [key, value] : dcache) {
+    if ((value.kind == DCacheKind::Normal) && (value.file->kind == DirectoryKind)) {
+      // Recursively remove all entries from child directories.
+      std::shared_ptr<Directory> childDir = value.file->cast<Directory>();
+      childDir->locked().removeAllCacheEntries();
+    }
+  }
+  dcache.clear();
+}
+
 // TODO: consider moving this to be `Backend::move` to avoid asymmetry between
 // the source and destination directories and/or taking `Directory::Handle`
 // arguments to prove that the directories have already been locked.
diff --git a/system/lib/wasmfs/file.h b/system/lib/wasmfs/file.h
index 039d265c21899..fa3d0d85b8b3f 100644
--- a/system/lib/wasmfs/file.h
+++ b/system/lib/wasmfs/file.h
@@ -423,6 +423,7 @@ class Directory::Handle : public File::Handle {
 
   [[nodiscard]] ssize_t getNumEntries();
   [[nodiscard]] MaybeEntries getEntries();
+  void removeAllCacheEntries();  
 };
 
 inline File::Handle File::locked() { return Handle(shared_from_this()); }
diff --git a/test/wasmfs/wasmfs_opfs.c b/test/wasmfs/wasmfs_opfs.c
index 8b1c3e6086458..3bd4c1b5abbad 100644
--- a/test/wasmfs/wasmfs_opfs.c
+++ b/test/wasmfs/wasmfs_opfs.c
@@ -202,15 +202,35 @@ int main(int argc, char* argv[]) {
   assert(err == 0);
   emscripten_console_log("moved file");
 
+  fd = open("/opfs/working/foo.txt", O_RDWR | O_CREAT | O_EXCL, 0777);
+  assert(fd > 0);
+  emscripten_console_log("created second OPFS file");
+  close(fd);
+
+
+  err = rename("/opfs/working", "/opfs/working2");
+  assert(err == 0);
+  err = access("/opfs/working", F_OK);
+  assert(err == -1);
+  err = access("/opfs/working2", F_OK);
+  assert(err == 0);
+  emscripten_console_log("moved directory");
+  
+  err = access("/opfs/working2/foo.txt", F_OK);
+  assert(err == 0);
+
+  err = unlink("/opfs/working2/foo.txt");
+  assert(err == 0);
+
   err = unlink("/opfs/foo.txt");
   assert(err == 0);
   err = access("/opfs/foo.txt", F_OK);
   assert(err == -1);
   emscripten_console_log("removed OPFS file");
 
-  err = rmdir("/opfs/working");
+  err = rmdir("/opfs/working2");
   assert(err == 0);
-  err = access("/opfs/working", F_OK);
+  err = access("/opfs/working2", F_OK);
   assert(err == -1);
   emscripten_console_log("removed OPFS directory");
 
@@ -224,9 +244,11 @@ void cleanup(void) {
 
   unlink("/opfs/working/foo.txt");
   rmdir("/opfs/working");
+  rmdir("/opfs/working2");
   unlink("/opfs/foo.txt");
 
   assert(access("/opfs/working/foo.txt", F_OK) != 0);
   assert(access("/opfs/working", F_OK) != 0);
+  assert(access("/opfs/working2", F_OK) != 0);
   assert(access("/opfs/foo.txt", F_OK) != 0);
 }
diff --git a/test/wasmfs/wasmfs_opfs_errors.c b/test/wasmfs/wasmfs_opfs_errors.c
index 019cd25317431..fdc7e7bb20cb7 100644
--- a/test/wasmfs/wasmfs_opfs_errors.c
+++ b/test/wasmfs/wasmfs_opfs_errors.c
@@ -122,25 +122,6 @@ int try_oob_write(void) {
   return 2;
 }
 
-EMSCRIPTEN_KEEPALIVE
-int try_rename_dir(void) {
-  int err = mkdir("/opfs/dir1", 0666);
-  if (err != 0) {
-    return 2;
-  }
-  err = rename("/opfs/dir1", "/opfs/dir2");
-  if (err == 0) {
-    return 1;
-  }
-  if (errno == EBUSY) {
-    rmdir("/opfs/dir1");
-    return 0;
-  }
-  emscripten_console_error(strerror(errno));
-  rmdir("/opfs/dir1");
-  return 2;
-}
-
 EMSCRIPTEN_KEEPALIVE
 void report_result(int result) {
   EM_ASM({ out(new Error().stack); });
diff --git a/test/wasmfs/wasmfs_opfs_errors_post.js b/test/wasmfs/wasmfs_opfs_errors_post.js
index e76675a899898..49069cb7376d7 100644
--- a/test/wasmfs/wasmfs_opfs_errors_post.js
+++ b/test/wasmfs/wasmfs_opfs_errors_post.js
@@ -66,9 +66,5 @@ async function run_test() {
           "nothing prevents it)";
   }
 
-  if (Module._try_rename_dir() != 0) {
-    throw "Did not get expected EBUSY while renaming directory";
-  }
-
   Module._report_result(0);
 }