diff --git a/src/library_wasmfs_opfs.js b/src/library_wasmfs_opfs.js
index 99ebc3da3c494..a0fe22b56b308 100644
--- a/src/library_wasmfs_opfs.js
+++ b/src/library_wasmfs_opfs.js
@@ -402,10 +402,14 @@ mergeInto(LibraryManager.library, {
   },
 
   _wasmfs_opfs_flush_access__deps: ['$wasmfsOPFSAccessHandles'],
-  _wasmfs_opfs_flush_access: async function(ctx, accessID) {
+  _wasmfs_opfs_flush_access: async function(ctx, accessID, errPtr) {
     let accessHandle = wasmfsOPFSAccessHandles.get(accessID);
-    // TODO: Error handling
-    await accessHandle.flush();
+    try {
+      await accessHandle.flush();
+    } catch {
+      let err = -{{{ cDefine('EIO') }}};
+      {{{ makeSetValue('errPtr', 0, 'err', 'i32') }}};
+    }
     _emscripten_proxy_finish(ctx);
   }
 });
diff --git a/system/lib/wasmfs/backends/node_backend.cpp b/system/lib/wasmfs/backends/node_backend.cpp
index 35f4d2169e382..9e9d7c4906e3e 100644
--- a/system/lib/wasmfs/backends/node_backend.cpp
+++ b/system/lib/wasmfs/backends/node_backend.cpp
@@ -179,7 +179,7 @@ class NodeFile : public DataFile {
     return nwritten;
   }
 
-  void flush() override {
+  int flush() override {
     WASMFS_UNREACHABLE("TODO: implement NodeFile::flush");
   }
 };
diff --git a/system/lib/wasmfs/backends/opfs_backend.cpp b/system/lib/wasmfs/backends/opfs_backend.cpp
index d69b82cca0637..23136ffc2a422 100644
--- a/system/lib/wasmfs/backends/opfs_backend.cpp
+++ b/system/lib/wasmfs/backends/opfs_backend.cpp
@@ -107,7 +107,7 @@ void _wasmfs_opfs_set_size_file(em_proxying_ctx* ctx,
                                 uint32_t size,
                                 int* err);
 
-void _wasmfs_opfs_flush_access(em_proxying_ctx* ctx, int access_id);
+void _wasmfs_opfs_flush_access(em_proxying_ctx* ctx, int access_id, int* err);
 
 } // extern "C"
 
@@ -313,11 +313,12 @@ class OPFSFile : public DataFile {
     return nwritten;
   }
 
-  void flush() override {
+  int flush() override {
+    int err = 0;
     switch (state.getKind()) {
       case OpenState::Access:
         proxy([&](auto ctx) {
-          _wasmfs_opfs_flush_access(ctx.ctx, state.getAccessID());
+          _wasmfs_opfs_flush_access(ctx.ctx, state.getAccessID(), &err);
         });
         break;
       case OpenState::Blob:
@@ -325,6 +326,7 @@ class OPFSFile : public DataFile {
       default:
         break;
     }
+    return err;
   }
 };
 
diff --git a/system/lib/wasmfs/backends/proxied_file_backend.cpp b/system/lib/wasmfs/backends/proxied_file_backend.cpp
index 7c46e75babe7d..07e78930d8a28 100644
--- a/system/lib/wasmfs/backends/proxied_file_backend.cpp
+++ b/system/lib/wasmfs/backends/proxied_file_backend.cpp
@@ -47,7 +47,7 @@ class ProxiedFile : public DataFile {
     return result;
   }
 
-  void flush() override {}
+  int flush() override { return 0; }
 
   // Querying the size of the Proxied File returns the size of the underlying
   // file given by the proxying mechanism.
diff --git a/system/lib/wasmfs/file.h b/system/lib/wasmfs/file.h
index 32937e714c284..84fe5635df8a6 100644
--- a/system/lib/wasmfs/file.h
+++ b/system/lib/wasmfs/file.h
@@ -146,8 +146,9 @@ class DataFile : public File {
   // opened. Returns 0 on success or a negative error code.
   virtual int setSize(size_t size) = 0;
 
-  // TODO: Design a proper API for flushing files.
-  virtual void flush() = 0;
+  // Sync the file data to the underlying persistent storage, if any. Returns 0
+  // on success or a negative error code.
+  virtual int flush() = 0;
 
 public:
   static constexpr FileKind expectedKind = File::DataFileKind;
@@ -327,7 +328,7 @@ class DataFile::Handle : public File::Handle {
   [[nodiscard]] int setSize(size_t size) { return getFile()->setSize(size); }
 
   // TODO: Design a proper API for flushing files.
-  void flush() { getFile()->flush(); }
+  [[nodiscard]] int flush() { return getFile()->flush(); }
 
   // This function loads preloaded files from JS Memory into this DataFile.
   // TODO: Make this virtual so specific backends can specialize it for better
diff --git a/system/lib/wasmfs/js_impl_backend.h b/system/lib/wasmfs/js_impl_backend.h
index 97b2d64974627..fe66b9a04de4e 100644
--- a/system/lib/wasmfs/js_impl_backend.h
+++ b/system/lib/wasmfs/js_impl_backend.h
@@ -94,7 +94,7 @@ class JSImplFile : public DataFile {
       getBackendIndex(), getFileIndex(), buf, len, offset);
   }
 
-  void flush() override {}
+  int flush() override { return 0; }
 
   size_t getSize() override {
     return _wasmfs_jsimpl_get_size(getBackendIndex(), getFileIndex());
diff --git a/system/lib/wasmfs/memory_backend.h b/system/lib/wasmfs/memory_backend.h
index 24c0b3138376f..7965ad49da43a 100644
--- a/system/lib/wasmfs/memory_backend.h
+++ b/system/lib/wasmfs/memory_backend.h
@@ -23,7 +23,7 @@ class MemoryFile : public DataFile {
   int close() override { return 0; }
   ssize_t write(const uint8_t* buf, size_t len, off_t offset) override;
   ssize_t read(uint8_t* buf, size_t len, off_t offset) override;
-  void flush() override {}
+  int flush() override { return 0; }
   size_t getSize() override { return buffer.size(); }
   int setSize(size_t size) override {
     buffer.resize(size);
diff --git a/system/lib/wasmfs/pipe_backend.h b/system/lib/wasmfs/pipe_backend.h
index e36778e6bfa60..105d93531e73f 100644
--- a/system/lib/wasmfs/pipe_backend.h
+++ b/system/lib/wasmfs/pipe_backend.h
@@ -44,7 +44,7 @@ class PipeFile : public DataFile {
     return len;
   }
 
-  void flush() override {}
+  int flush() override { return 0; }
 
   size_t getSize() override { return data->size(); }
 
diff --git a/system/lib/wasmfs/proxied_async_js_impl_backend.h b/system/lib/wasmfs/proxied_async_js_impl_backend.h
index 0aad7e7fbc003..025c85abbcca1 100644
--- a/system/lib/wasmfs/proxied_async_js_impl_backend.h
+++ b/system/lib/wasmfs/proxied_async_js_impl_backend.h
@@ -106,7 +106,7 @@ class ProxiedAsyncJSImplFile : public DataFile {
     return result;
   }
 
-  void flush() override {}
+  int flush() override { return 0; }
 
   size_t getSize() override {
     size_t result;
diff --git a/system/lib/wasmfs/special_files.cpp b/system/lib/wasmfs/special_files.cpp
index de7c3cac15fea..a00eb72c10fe4 100644
--- a/system/lib/wasmfs/special_files.cpp
+++ b/system/lib/wasmfs/special_files.cpp
@@ -28,7 +28,7 @@ class NullFile : public DataFile {
 
   ssize_t read(uint8_t* buf, size_t len, off_t offset) override { return 0; }
 
-  void flush() override {}
+  int flush() override { return 0; }
   size_t getSize() override { return 0; }
   int setSize(size_t size) override { return -EPERM; }
 
@@ -49,7 +49,7 @@ class StdinFile : public DataFile {
     abort();
   };
 
-  void flush() override {}
+  int flush() override { return 0; }
   size_t getSize() override { return 0; }
   int setSize(size_t size) override { return -EPERM; }
 
@@ -69,12 +69,13 @@ class WritingStdFile : public DataFile {
     return -__WASI_ERRNO_INVAL;
   };
 
-  void flush() override {
+  int flush() override {
     // Write a null to flush the output if we have content.
     if (!writeBuffer.empty()) {
       const uint8_t nothing = '\0';
       write(&nothing, 1, 0);
     }
+    return 0;
   }
 
   size_t getSize() override { return 0; }
@@ -150,7 +151,7 @@ class RandomFile : public DataFile {
     return len;
   };
 
-  void flush() override {}
+  int flush() override { return 0; }
   size_t getSize() override { return 0; }
   int setSize(size_t size) override { return -EPERM; }
 
diff --git a/system/lib/wasmfs/syscalls.cpp b/system/lib/wasmfs/syscalls.cpp
index 09aa9ab858161..92b5b8356fa13 100644
--- a/system/lib/wasmfs/syscalls.cpp
+++ b/system/lib/wasmfs/syscalls.cpp
@@ -292,7 +292,8 @@ __wasi_errno_t __wasi_fd_sync(__wasi_fd_t fd) {
   // way. TODO: in the future we may want syncing of directories.
   auto dataFile = openFile->locked().getFile()->dynCast<DataFile>();
   if (dataFile) {
-    dataFile->locked().flush();
+    // Translate to WASI standard of positive return codes.
+    return -dataFile->locked().flush();
   }
 
   return __WASI_ERRNO_SUCCESS;
diff --git a/system/lib/wasmfs/wasmfs.cpp b/system/lib/wasmfs/wasmfs.cpp
index 011896b23bdd3..6cdf062836ff9 100644
--- a/system/lib/wasmfs/wasmfs.cpp
+++ b/system/lib/wasmfs/wasmfs.cpp
@@ -58,8 +58,8 @@ WasmFS::~WasmFS() {
   // Note that we lock here, although strictly speaking it is unnecessary given
   // that we are in the destructor of WasmFS: nothing can possibly be running
   // on files at this time.
-  SpecialFiles::getStdout()->locked().flush();
-  SpecialFiles::getStderr()->locked().flush();
+  (void)SpecialFiles::getStdout()->locked().flush();
+  (void)SpecialFiles::getStderr()->locked().flush();
 
   // Break the reference cycle caused by the root directory being its own
   // parent.