diff --git a/Source/Core/Core/Boot/Boot_WiiWAD.cpp b/Source/Core/Core/Boot/Boot_WiiWAD.cpp
index 5ecfd48471..111f87de3b 100644
--- a/Source/Core/Core/Boot/Boot_WiiWAD.cpp
+++ b/Source/Core/Core/Boot/Boot_WiiWAD.cpp
@@ -49,7 +49,6 @@ static void CreateVirtualFATFilesystem(std::shared_ptr<IOS::HLE::FS::FileSystem>
   // write the final 0 to 0 file from the second FAT to 20 MiB
   data[CDB_SIZE - 1] = 0;
   fs->WriteFile(*fd, data.data(), static_cast<u32>(data.size()));
-  fs->Close(*fd);
 }
 
 bool CBoot::BootNANDTitle(const u64 title_id)
diff --git a/Source/Core/Core/IOS/FS/FileSystem.cpp b/Source/Core/Core/IOS/FS/FileSystem.cpp
index 50aa764ee7..f3910c3374 100644
--- a/Source/Core/Core/IOS/FS/FileSystem.cpp
+++ b/Source/Core/Core/IOS/FS/FileSystem.cpp
@@ -4,6 +4,7 @@
 
 #include "Core/IOS/FS/FileSystem.h"
 
+#include "Common/Assert.h"
 #include "Core/IOS/FS/HostBackend/FS.h"
 
 namespace IOS::HLE::FS
@@ -13,6 +14,35 @@ std::unique_ptr<FileSystem> MakeFileSystem()
   return std::make_unique<HostFileSystem>();
 }
 
+FileHandle::FileHandle(FileSystem* fs, Fd fd) : m_fs{fs}, m_fd{fd}
+{
+}
+
+FileHandle::FileHandle(FileHandle&& other) : m_fs{other.m_fs}, m_fd{other.m_fd}
+{
+  other.m_fd.reset();
+}
+
+FileHandle& FileHandle::operator=(FileHandle&& other)
+{
+  if (*this != other)
+    *this = std::move(other);
+  return *this;
+}
+
+FileHandle::~FileHandle()
+{
+  if (m_fd && m_fs)
+    ASSERT(m_fs->Close(*m_fd) == FS::ResultCode::Success);
+}
+
+Fd FileHandle::Release()
+{
+  const Fd fd = m_fd.value();
+  m_fd.reset();
+  return fd;
+}
+
 void FileSystem::Init()
 {
   if (Delete(0, 0, "/tmp") == ResultCode::Success)
diff --git a/Source/Core/Core/IOS/FS/FileSystem.h b/Source/Core/Core/IOS/FS/FileSystem.h
index 94fc430230..25894a60b0 100644
--- a/Source/Core/Core/IOS/FS/FileSystem.h
+++ b/Source/Core/Core/IOS/FS/FileSystem.h
@@ -5,6 +5,7 @@
 #pragma once
 
 #include <memory>
+#include <optional>
 #include <string>
 #include <vector>
 
@@ -96,6 +97,26 @@ struct FileStatus
   u32 size;
 };
 
+class FileSystem;
+class FileHandle final
+{
+public:
+  FileHandle(FileSystem* fs, Fd fd);
+  FileHandle(FileHandle&&);
+  ~FileHandle();
+  FileHandle(const FileHandle&) = delete;
+  FileHandle& operator=(const FileHandle&) = delete;
+  FileHandle& operator=(FileHandle&&);
+
+  operator Fd() const { return m_fd.value(); }
+  /// Release the FD so that it is not automatically closed.
+  Fd Release();
+
+private:
+  FileSystem* m_fs;
+  std::optional<Fd> m_fd;
+};
+
 class FileSystem
 {
 public:
@@ -106,8 +127,8 @@ public:
   /// Format the file system.
   virtual ResultCode Format(Uid uid) = 0;
 
-  /// Get a file descriptor for accessing a file.
-  virtual Result<Fd> OpenFile(Uid uid, Gid gid, const std::string& path, Mode mode) = 0;
+  /// Get a file descriptor for accessing a file. The FD will be automatically closed after use.
+  virtual Result<FileHandle> OpenFile(Uid uid, Gid gid, const std::string& path, Mode mode) = 0;
   /// Close a file descriptor.
   virtual ResultCode Close(Fd fd) = 0;
   /// Read `size` bytes from the file descriptor. Returns the number of bytes read.
diff --git a/Source/Core/Core/IOS/FS/FileSystemProxy.cpp b/Source/Core/Core/IOS/FS/FileSystemProxy.cpp
index e73d502f8a..75d0c6c6b4 100644
--- a/Source/Core/Core/IOS/FS/FileSystemProxy.cpp
+++ b/Source/Core/Core/IOS/FS/FileSystemProxy.cpp
@@ -70,13 +70,13 @@ IPCCommandResult FS::Open(const OpenRequest& request)
     return GetDefaultReply(IPC_SUCCESS);
   }
 
-  const auto backend_fd = m_ios.GetFS()->OpenFile(request.uid, request.gid, request.path,
-                                                  static_cast<Mode>(request.flags & 3));
+  auto backend_fd = m_ios.GetFS()->OpenFile(request.uid, request.gid, request.path,
+                                            static_cast<Mode>(request.flags & 3));
   LogResult(StringFromFormat("OpenFile(%s)", request.path.c_str()), backend_fd);
   if (!backend_fd)
     return GetFSReply(ConvertResult(backend_fd.Error()));
 
-  m_fd_map[request.fd] = {request.gid, request.uid, *backend_fd};
+  m_fd_map[request.fd] = {request.gid, request.uid, backend_fd->Release()};
   std::strncpy(m_fd_map[request.fd].name.data(), request.path.c_str(), 64);
   return GetFSReply(IPC_SUCCESS);
 }
diff --git a/Source/Core/Core/IOS/FS/HostBackend/FS.h b/Source/Core/Core/IOS/FS/HostBackend/FS.h
index cb7283d1f0..60f5d4dfd4 100644
--- a/Source/Core/Core/IOS/FS/HostBackend/FS.h
+++ b/Source/Core/Core/IOS/FS/HostBackend/FS.h
@@ -30,7 +30,7 @@ public:
 
   ResultCode Format(Uid uid) override;
 
-  Result<Fd> OpenFile(Uid uid, Gid gid, const std::string& path, Mode mode) override;
+  Result<FileHandle> OpenFile(Uid uid, Gid gid, const std::string& path, Mode mode) override;
   ResultCode Close(Fd fd) override;
   Result<u32> ReadBytesFromFile(Fd fd, u8* ptr, u32 size) override;
   Result<u32> WriteBytesToFile(Fd fd, const u8* ptr, u32 size) override;
diff --git a/Source/Core/Core/IOS/FS/HostBackend/File.cpp b/Source/Core/Core/IOS/FS/HostBackend/File.cpp
index 405c877c45..661413300d 100644
--- a/Source/Core/Core/IOS/FS/HostBackend/File.cpp
+++ b/Source/Core/Core/IOS/FS/HostBackend/File.cpp
@@ -57,7 +57,7 @@ std::shared_ptr<File::IOFile> HostFileSystem::OpenHostFile(const std::string& ho
   return file;
 }
 
-Result<Fd> HostFileSystem::OpenFile(Uid uid, Gid gid, const std::string& path, Mode mode)
+Result<FileHandle> HostFileSystem::OpenFile(Uid, Gid, const std::string& path, Mode mode)
 {
   Handle* handle = AssignFreeHandle();
   if (!handle)
@@ -74,7 +74,7 @@ Result<Fd> HostFileSystem::OpenFile(Uid uid, Gid gid, const std::string& path, M
   handle->wii_path = path;
   handle->mode = mode;
   handle->file_offset = 0;
-  return ConvertHandleToFd(handle);
+  return FileHandle{this, ConvertHandleToFd(handle)};
 }
 
 ResultCode HostFileSystem::Close(Fd fd)