diff --git a/Source/Core/Common/CMakeLists.txt b/Source/Core/Common/CMakeLists.txt
index cf209ab2279..e833893a9de 100644
--- a/Source/Core/Common/CMakeLists.txt
+++ b/Source/Core/Common/CMakeLists.txt
@@ -52,6 +52,8 @@ add_library(common
   Debug/Threads.h
   Debug/Watches.cpp
   Debug/Watches.h
+  DirectIOFile.cpp
+  DirectIOFile.h
   DynamicLibrary.cpp
   DynamicLibrary.h
   ENet.cpp
diff --git a/Source/Core/Common/DirectIOFile.cpp b/Source/Core/Common/DirectIOFile.cpp
new file mode 100644
index 00000000000..d5e805529de
--- /dev/null
+++ b/Source/Core/Common/DirectIOFile.cpp
@@ -0,0 +1,372 @@
+// Copyright 2025 Dolphin Emulator Project
+// SPDX-License-Identifier: GPL-2.0-or-later
+
+#include "Common/DirectIOFile.h"
+
+#include <utility>
+
+#if defined(_WIN32)
+#include <windows.h>
+
+#include <cstring>
+
+#include "Common/Buffer.h"
+#include "Common/CommonFuncs.h"
+#include "Common/MathUtil.h"
+#include "Common/StringUtil.h"
+#else
+#include <string>
+
+#include <fcntl.h>
+#include <sys/stat.h>
+#include <unistd.h>
+
+#ifdef ANDROID
+#include "jni/AndroidCommon/AndroidCommon.h"
+
+#include "Common/Lazy.h"
+#endif
+
+#include "Common/FileUtil.h"
+#endif
+
+#include "Common/Assert.h"
+
+namespace File
+{
+DirectIOFile::DirectIOFile() = default;
+
+DirectIOFile::~DirectIOFile()
+{
+  Close();
+}
+
+DirectIOFile::DirectIOFile(const DirectIOFile& other)
+{
+  *this = other.Duplicate();
+}
+
+DirectIOFile& DirectIOFile::operator=(const DirectIOFile& other)
+{
+  return *this = other.Duplicate();
+}
+
+DirectIOFile::DirectIOFile(DirectIOFile&& other)
+{
+  Swap(other);
+}
+
+DirectIOFile& DirectIOFile::operator=(DirectIOFile&& other)
+{
+  Close();
+  Swap(other);
+  return *this;
+}
+
+DirectIOFile::DirectIOFile(const std::string& path, AccessMode access_mode, OpenMode open_mode)
+{
+  Open(path, access_mode, open_mode);
+}
+
+bool DirectIOFile::Open(const std::string& path, AccessMode access_mode, OpenMode open_mode)
+{
+  ASSERT(!IsOpen());
+
+  if (open_mode == OpenMode::Default)
+    open_mode = (access_mode == AccessMode::Write) ? OpenMode::Truncate : OpenMode::Existing;
+
+  // This is not a sensible combination. Fail here to not rely on OS-specific behaviors.
+  if (access_mode == AccessMode::Read && open_mode == OpenMode::Truncate)
+    return false;
+
+#if defined(_WIN32)
+  DWORD desired_access = GENERIC_READ | GENERIC_WRITE;
+  if (access_mode == AccessMode::Read)
+    desired_access = GENERIC_READ;
+  else if (access_mode == AccessMode::Write)
+    desired_access = GENERIC_WRITE;
+
+  // Allow deleting and renaming through our handle.
+  desired_access |= DELETE;
+
+  // All sharing is allowed to more closely match default behavior on other OSes.
+  constexpr DWORD share_mode = FILE_SHARE_DELETE | FILE_SHARE_READ | FILE_SHARE_WRITE;
+
+  DWORD creation_disposition = OPEN_ALWAYS;
+  if (open_mode == OpenMode::Truncate)
+    creation_disposition = CREATE_ALWAYS;
+  else if (open_mode == OpenMode::Create)
+    creation_disposition = CREATE_NEW;
+  else if (open_mode == OpenMode::Existing)
+    creation_disposition = OPEN_EXISTING;
+
+  m_handle = CreateFile(UTF8ToTStr(path).c_str(), desired_access, share_mode, nullptr,
+                        creation_disposition, FILE_ATTRIBUTE_NORMAL, nullptr);
+  if (!IsOpen())
+    WARN_LOG_FMT(COMMON, "CreateFile: {}", Common::GetLastErrorString());
+
+#else
+#if defined(ANDROID)
+  if (IsPathAndroidContent(path))
+  {
+    // Android documentation says that "w" may or may not truncate.
+    // In case it does, we'll use "rw" when we don't want truncation.
+    // This wrongly enables read access when we don't need it.
+    if (access_mode == AccessMode::Write && open_mode != OpenMode::Truncate)
+      access_mode = AccessMode::ReadAndWrite;
+
+    std::string open_mode_str = "rw";
+    if (access_mode == AccessMode::Read)
+      open_mode_str = "r";
+    else if (access_mode == AccessMode::Write)
+      open_mode_str = "w";
+
+    // FYI: File::Exists can be slow on Android.
+    Common::Lazy<bool> file_exists{[&] { return Exists(path); }};
+
+    // A few features are emulated in a non-atomic manner.
+    if (open_mode == OpenMode::Existing)
+    {
+      if (access_mode != AccessMode::Read && !*file_exists)
+        return false;
+    }
+    else
+    {
+      if (open_mode == OpenMode::Truncate)
+        open_mode_str += 't';
+      else if (open_mode == OpenMode::Create && *file_exists)
+        return false;
+
+      // Modes other than `Existing` may create a file, but "r" won't do that automatically.
+      if (access_mode == AccessMode::Read && !*file_exists)
+        CreateEmptyFile(path);
+    }
+
+    m_fd = OpenAndroidContent(path, open_mode_str);
+
+    return IsOpen();
+  }
+#endif
+  int flags = O_RDWR;
+  if (access_mode == AccessMode::Read)
+    flags = O_RDONLY;
+  else if (access_mode == AccessMode::Write)
+    flags = O_WRONLY;
+
+  if (open_mode == OpenMode::Truncate)
+    flags |= O_CREAT | O_TRUNC;
+  else if (open_mode == OpenMode::Create)
+    flags |= O_CREAT | O_EXCL;
+  else if (open_mode != OpenMode::Existing)
+    flags |= O_CREAT;
+
+  m_fd = open(path.c_str(), flags, 0666);
+
+#endif
+
+  return IsOpen();
+}
+
+bool DirectIOFile::Close()
+{
+  if (!IsOpen())
+    return false;
+
+  m_current_offset = 0;
+
+#if defined(_WIN32)
+  return CloseHandle(std::exchange(m_handle, INVALID_HANDLE_VALUE)) != 0;
+#else
+  return close(std::exchange(m_fd, -1)) == 0;
+#endif
+}
+
+bool DirectIOFile::IsOpen() const
+{
+#if defined(_WIN32)
+  return m_handle != INVALID_HANDLE_VALUE;
+#else
+  return m_fd != -1;
+#endif
+}
+
+#if defined(_WIN32)
+template <auto* TransferFunc>
+static bool OverlappedTransfer(HANDLE handle, u64 offset, auto* data_ptr, u64 size)
+{
+  // ReadFile/WriteFile take a 32bit size so we must loop to handle our 64bit size.
+  while (true)
+  {
+    OVERLAPPED overlapped{};
+    overlapped.Offset = DWORD(offset);
+    overlapped.OffsetHigh = DWORD(offset >> 32);
+
+    DWORD bytes_transferred{};
+    if (TransferFunc(handle, data_ptr, MathUtil::SaturatingCast<DWORD>(size), &bytes_transferred,
+                     &overlapped) == 0)
+    {
+      ERROR_LOG_FMT(COMMON, "OverlappedTransfer: {}", Common::GetLastErrorString());
+      return false;
+    }
+
+    size -= bytes_transferred;
+
+    if (size == 0)
+      return true;
+
+    offset += bytes_transferred;
+    data_ptr += bytes_transferred;
+  }
+}
+#endif
+
+bool DirectIOFile::OffsetRead(u64 offset, u8* out_ptr, u64 size)
+{
+#if defined(_WIN32)
+  return OverlappedTransfer<ReadFile>(m_handle, offset, out_ptr, size);
+#else
+  return pread(m_fd, out_ptr, size, off_t(offset)) == ssize_t(size);
+#endif
+}
+
+bool DirectIOFile::OffsetWrite(u64 offset, const u8* in_ptr, u64 size)
+{
+#if defined(_WIN32)
+  return OverlappedTransfer<WriteFile>(m_handle, offset, in_ptr, size);
+#else
+  return pwrite(m_fd, in_ptr, size, off_t(offset)) == ssize_t(size);
+#endif
+}
+
+u64 DirectIOFile::GetSize() const
+{
+#if defined(_WIN32)
+  LARGE_INTEGER result{};
+  if (GetFileSizeEx(m_handle, &result) != 0)
+    return result.QuadPart;
+#else
+  struct stat st{};
+  if (fstat(m_fd, &st) == 0)
+    return st.st_size;
+#endif
+
+  return 0;
+}
+
+bool DirectIOFile::Seek(s64 offset, SeekOrigin origin)
+{
+  if (!IsOpen())
+    return false;
+
+  u64 reference_pos = 0;
+  switch (origin)
+  {
+  case SeekOrigin::Current:
+    reference_pos = m_current_offset;
+    break;
+  case SeekOrigin::End:
+    reference_pos = GetSize();
+    break;
+  default:
+    break;
+  }
+
+  // Don't let our current offset underflow.
+  if (offset < 0 && u64(-offset) > reference_pos)
+    return false;
+
+  m_current_offset = reference_pos + offset;
+  return true;
+}
+
+bool DirectIOFile::Flush()
+{
+#if defined(_WIN32)
+  return FlushFileBuffers(m_handle) != 0;
+#else
+  return fsync(m_fd) == 0;
+#endif
+}
+
+void DirectIOFile::Swap(DirectIOFile& other)
+{
+#if defined(_WIN32)
+  std::swap(m_handle, other.m_handle);
+#else
+  std::swap(m_fd, other.m_fd);
+#endif
+  std::swap(m_current_offset, other.m_current_offset);
+}
+
+DirectIOFile DirectIOFile::Duplicate() const
+{
+  DirectIOFile result;
+
+  if (!IsOpen())
+    return result;
+
+#if defined(_WIN32)
+  const auto current_process = GetCurrentProcess();
+  if (DuplicateHandle(current_process, m_handle, current_process, &result.m_handle, 0, FALSE,
+                      DUPLICATE_SAME_ACCESS) == 0)
+  {
+    ERROR_LOG_FMT(COMMON, "DuplicateHandle: {}", Common::GetLastErrorString());
+  }
+#else
+  result.m_fd = dup(m_fd);
+#endif
+
+  ASSERT(result.IsOpen());
+
+  result.m_current_offset = m_current_offset;
+
+  return result;
+}
+
+bool Resize(DirectIOFile& file, u64 size)
+{
+#if defined(_WIN32)
+  // This operation is not "atomic", but it's the only thing we're using the file pointer for.
+  // Concurrent `Resize` would need some external synchronization to prevent race regardless.
+  const LARGE_INTEGER distance{.QuadPart = LONGLONG(size)};
+  return (SetFilePointerEx(file.GetHandle(), distance, nullptr, FILE_BEGIN) != 0) &&
+         (SetEndOfFile(file.GetHandle()) != 0);
+#else
+  return ftruncate(file.GetHandle(), off_t(size)) == 0;
+#endif
+}
+
+bool Rename(DirectIOFile& file, const std::string& source_path [[maybe_unused]],
+            const std::string& destination_path)
+{
+#if defined(_WIN32)
+  const auto dest_name = UTF8ToWString(destination_path);
+  const auto dest_name_byte_size = DWORD(dest_name.size() * sizeof(WCHAR));
+  FILE_RENAME_INFO info{
+      .ReplaceIfExists = TRUE,
+      .FileNameLength = dest_name_byte_size,  // The size in bytes, not including null termination.
+  };
+  constexpr auto filename_struct_offset = offsetof(FILE_RENAME_INFO, FileName);
+  Common::UniqueBuffer<u8> buffer(filename_struct_offset + dest_name_byte_size + sizeof(WCHAR));
+  std::memcpy(buffer.data(), &info, filename_struct_offset);
+  std::memcpy(buffer.data() + filename_struct_offset, dest_name.c_str(),
+              dest_name_byte_size + sizeof(WCHAR));
+  return SetFileInformationByHandle(file.GetHandle(), FileRenameInfo, buffer.data(),
+                                    DWORD(buffer.size())) != 0;
+#else
+  return file.IsOpen() && Rename(source_path, destination_path);
+#endif
+}
+
+bool Delete(DirectIOFile& file, const std::string& filename)
+{
+#if defined(_WIN32)
+  FILE_DISPOSITION_INFO info{.DeleteFile = TRUE};
+  return SetFileInformationByHandle(file.GetHandle(), FileDispositionInfo, &info, sizeof(info)) !=
+         0;
+#else
+  return file.IsOpen() && Delete(filename, IfAbsentBehavior::NoConsoleWarning);
+#endif
+}
+
+}  // namespace File
diff --git a/Source/Core/Common/DirectIOFile.h b/Source/Core/Common/DirectIOFile.h
new file mode 100644
index 00000000000..79a5e68a2c1
--- /dev/null
+++ b/Source/Core/Common/DirectIOFile.h
@@ -0,0 +1,150 @@
+// Copyright 2025 Dolphin Emulator Project
+// SPDX-License-Identifier: GPL-2.0-or-later
+
+#pragma once
+
+#include <span>
+#include <string>
+
+#include "Common/CommonTypes.h"
+#include "Common/IOFile.h"
+
+namespace File
+{
+enum class AccessMode
+{
+  Read,
+  Write,
+  ReadAndWrite,
+};
+
+enum class OpenMode
+{
+  // Based on the provided `AccessMode`.
+  // Read: Existing.
+  // Write: Truncate.
+  // ReadAndWrite: Existing.
+  Default,
+
+  // Either create a new file or open an existing file.
+  Always,
+
+  // Like `Always`, but also erase the contents of an existing file.
+  Truncate,
+
+  // Require a file to already exist. Fail otherwise.
+  Existing,
+
+  // Require a new file be created. Fail if one already exists.
+  Create,
+};
+
+// This file wrapper avoids use of the underlying system file position.
+// It keeps track of its own file position and read/write calls directly use it.
+// This makes copied handles entirely thread safe.
+class DirectIOFile final
+{
+public:
+  DirectIOFile();
+  ~DirectIOFile();
+
+  // Copies and moves are allowed.
+  DirectIOFile(const DirectIOFile&);
+  DirectIOFile& operator=(const DirectIOFile&);
+  DirectIOFile(DirectIOFile&&);
+  DirectIOFile& operator=(DirectIOFile&&);
+
+  explicit DirectIOFile(const std::string& path, AccessMode access_mode,
+                        OpenMode open_mode = OpenMode::Default);
+
+  bool Open(const std::string& path, AccessMode access_mode,
+            OpenMode open_mode = OpenMode::Default);
+
+  bool Close();
+
+  bool IsOpen() const;
+
+  // An offset from the start of the file may be specified directly.
+  // These explicit offset versions entirely ignore the current file position.
+  // They are thread safe, even when used on the same object.
+
+  bool OffsetRead(u64 offset, u8* out_ptr, u64 size);
+  bool OffsetRead(u64 offset, std::span<u8> out_data)
+  {
+    return OffsetRead(offset, out_data.data(), out_data.size());
+  }
+  bool OffsetWrite(u64 offset, const u8* in_ptr, u64 size);
+  bool OffsetWrite(auto offset, std::span<const u8> in_data)
+  {
+    return OffsetWrite(offset, in_data.data(), in_data.size());
+  }
+
+  // These Read/Write functions advance the current position on success.
+
+  bool Read(u8* out_ptr, u64 size)
+  {
+    if (!OffsetRead(m_current_offset, out_ptr, size))
+      return false;
+    m_current_offset += size;
+    return true;
+  }
+  bool Read(std::span<u8> out_data) { return Read(out_data.data(), out_data.size()); }
+
+  bool Write(const u8* in_ptr, u64 size)
+  {
+    if (!OffsetWrite(m_current_offset, in_ptr, size))
+      return false;
+    m_current_offset += size;
+    return true;
+  }
+  bool Write(std::span<const u8> in_data) { return Write(in_data.data(), in_data.size()); }
+
+  // Returns 0 on error.
+  u64 GetSize() const;
+
+  bool Seek(s64 offset, SeekOrigin origin);
+
+  // Returns 0 when not open.
+  u64 Tell() const { return m_current_offset; }
+
+  bool Flush();
+
+  auto GetHandle() const
+  {
+#if defined(_WIN32)
+    return m_handle;
+#else
+    return m_fd;
+#endif
+  }
+
+private:
+  void Swap(DirectIOFile& other);
+  DirectIOFile Duplicate() const;
+
+#if defined(_WIN32)
+  // A workaround to avoid including <windows.h> in this header.
+  // HANDLE is just void* and INVALID_HANDLE_VALUE is -1.
+  using HandleType = void*;
+  HandleType m_handle{HandleType(-1)};
+#else
+  using HandleType = int;
+  HandleType m_fd{-1};
+#endif
+
+  u64 m_current_offset{};
+};
+
+// These take an open file handle to avoid failures from other processes trying to open our files.
+// This is mainly an issue on Windows.
+
+bool Resize(DirectIOFile& file, u64 size);
+
+// Attempts to replace a destination file if one already exists.
+// Note: Windows uses `file`. Elsewhere uses `source_path`, but `file` is checked for openness.
+bool Rename(DirectIOFile& file, const std::string& source_path,
+            const std::string& destination_path);
+// Note: Ditto, only Windows actually uses the file handle. Provide both.
+bool Delete(DirectIOFile& file, const std::string& filename);
+
+}  // namespace File
diff --git a/Source/Core/DolphinLib.props b/Source/Core/DolphinLib.props
index 32f76c8d014..17e44675ac2 100644
--- a/Source/Core/DolphinLib.props
+++ b/Source/Core/DolphinLib.props
@@ -51,6 +51,7 @@
     <ClInclude Include="Common\Debug\MemoryPatches.h" />
     <ClInclude Include="Common\Debug\Threads.h" />
     <ClInclude Include="Common\Debug\Watches.h" />
+    <ClInclude Include="Common\DirectIOFile.h" />
     <ClInclude Include="Common\DynamicLibrary.h" />
     <ClInclude Include="Common\ENet.h" />
     <ClInclude Include="Common\EnumFormatter.h" />
@@ -820,6 +821,7 @@
     <ClCompile Include="Common\Crypto\SHA1.cpp" />
     <ClCompile Include="Common\Debug\MemoryPatches.cpp" />
     <ClCompile Include="Common\Debug\Watches.cpp" />
+    <ClCompile Include="Common\DirectIOFile.cpp" />
     <ClCompile Include="Common\DynamicLibrary.cpp" />
     <ClCompile Include="Common\ENet.cpp" />
     <ClCompile Include="Common\FatFsUtil.cpp" />
diff --git a/Source/UnitTests/Common/FileUtilTest.cpp b/Source/UnitTests/Common/FileUtilTest.cpp
index 6b3f1168d24..bfdc9128f6b 100644
--- a/Source/UnitTests/Common/FileUtilTest.cpp
+++ b/Source/UnitTests/Common/FileUtilTest.cpp
@@ -1,9 +1,15 @@
 // Copyright 2020 Dolphin Emulator Project
 // SPDX-License-Identifier: GPL-2.0-or-later
 
+#include <algorithm>
 #include <array>
+#include <latch>
+#include <thread>
+
 #include <gtest/gtest.h>
 
+#include "Common/BitUtils.h"
+#include "Common/DirectIOFile.h"
 #include "Common/FileUtil.h"
 
 class FileUtilTest : public testing::Test
@@ -147,3 +153,262 @@ TEST_F(FileUtilTest, CreateFullPath)
   EXPECT_FALSE(File::CreateFullPath(p3file + "/"));
   EXPECT_TRUE(File::IsFile(p3file));
 }
+
+TEST_F(FileUtilTest, DirectIOFile)
+{
+  static constexpr std::array<u8, 3> u8_test_data = {42, 7, 99};
+  static constexpr std::array<u16, 3> u16_test_data = {0xdead, 0xbeef, 0xf00d};
+
+  static constexpr int u16_data_offset = 73;
+
+  File::DirectIOFile file;
+  EXPECT_FALSE(file.IsOpen());
+
+  // Read mode fails with a non-existing file.
+  EXPECT_FALSE(file.Open(m_file_path, File::AccessMode::Read));
+
+  std::array<u8, u8_test_data.size()> u8_buffer = {};
+
+  // Everything fails when a file isn't open.
+  EXPECT_FALSE(file.Write(u8_buffer));
+  EXPECT_FALSE(file.Read(u8_buffer));
+  EXPECT_FALSE(file.Flush());
+  EXPECT_FALSE(file.Seek(12, File::SeekOrigin::Begin));
+  EXPECT_EQ(file.Tell(), 0);
+  EXPECT_EQ(file.GetSize(), 0);
+
+  // Fail to open non-existing file.
+  EXPECT_FALSE(file.Open(m_file_path, File::AccessMode::ReadAndWrite));
+  EXPECT_FALSE(file.Open(m_file_path, File::AccessMode::Read, File::OpenMode::Existing));
+  EXPECT_FALSE(file.Open(m_file_path, File::AccessMode::Write, File::OpenMode::Existing));
+
+  // Read mode can create files
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Read, File::OpenMode::Create));
+  EXPECT_TRUE(file.Close());
+
+  // Open a file for writing.
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Write, File::OpenMode::Always));
+  EXPECT_TRUE(file.Flush());
+  EXPECT_TRUE(file.IsOpen());
+
+  // Note: Double Open() currently ASSERTs. It's not obvious if that should succeed or fail.
+
+  EXPECT_TRUE(file.Close());
+  EXPECT_FALSE(file.Open(m_file_path, File::AccessMode::Write, File::OpenMode::Create));
+
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Write, File::OpenMode::Existing));
+  EXPECT_TRUE(file.Close());
+
+  // Rename, Resize, and Delete fail with a closed handle.
+  EXPECT_FALSE(Rename(file, m_file_path, "fail"));
+  EXPECT_FALSE(Resize(file, 72));
+  EXPECT_FALSE(Delete(file, m_file_path));
+  EXPECT_TRUE(File::Exists(m_file_path));
+
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Write));
+
+  EXPECT_TRUE(file.Write(u8_buffer.data(), 0));  // write of 0 succeeds.
+  EXPECT_FALSE(file.Read(u8_buffer.data(), 0));  // read of 0 (in write mode) fails.
+
+  // Resize through handle works.
+  EXPECT_TRUE(Resize(file, 1));
+  EXPECT_EQ(file.GetSize(), 1);
+  file.Close();
+
+  // Write truncates by default.
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Write));
+  EXPECT_EQ(file.GetSize(), 0);
+
+  EXPECT_TRUE(file.Write(u8_test_data));
+  EXPECT_EQ(file.GetSize(), u8_test_data.size());  // size changed
+  EXPECT_EQ(file.Tell(), u8_test_data.size());     // file position changed
+
+  // Relative seek works.
+  EXPECT_TRUE(file.Seek(0, File::SeekOrigin::End));
+  EXPECT_EQ(file.Tell(), file.GetSize());
+  EXPECT_TRUE(file.Seek(-int(u8_test_data.size()), File::SeekOrigin::Current));
+  EXPECT_EQ(file.Tell(), 0);
+
+  // Read while in "write mode" fails
+  EXPECT_FALSE(file.Read(u8_buffer));
+  EXPECT_EQ(file.Tell(), 0);
+
+  // Seeking past the end works.
+  EXPECT_TRUE(file.Seek(u16_data_offset, File::SeekOrigin::Begin));
+  EXPECT_EQ(file.Tell(), u16_data_offset);
+  EXPECT_EQ(file.GetSize(), u8_test_data.size());  // no change in size
+
+  static constexpr u64 final_file_size = u16_data_offset + sizeof(u16_test_data);
+
+  // Size changes after write.
+  EXPECT_TRUE(file.Write(Common::AsU8Span(u16_test_data)));
+  EXPECT_EQ(file.GetSize(), final_file_size);
+
+  // Seek before begin fails.
+  EXPECT_FALSE(file.Seek(-1, File::SeekOrigin::Begin));
+  EXPECT_EQ(file.Tell(), file.GetSize());  // unchanged position
+
+  EXPECT_TRUE(file.Close());
+  EXPECT_FALSE(file.IsOpen());
+
+  EXPECT_EQ(file.Tell(), 0);
+  EXPECT_EQ(file.GetSize(), 0);
+
+  EXPECT_FALSE(file.Close());  // Double close fails.
+
+  // Open file for reading.
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Read, File::OpenMode::Always));
+  EXPECT_TRUE(file.Close());
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Read));
+
+  static constexpr int big_offset = 999;
+
+  // We can seek beyond the end.
+  EXPECT_TRUE(file.Seek(big_offset, File::SeekOrigin::End));
+  EXPECT_EQ(file.Tell(), file.GetSize() + big_offset);
+
+  // Resize through handle fails when in read mode.
+  EXPECT_FALSE(Resize(file, big_offset));
+  EXPECT_EQ(file.GetSize(), final_file_size);
+
+  constexpr size_t thread_count = 4;
+
+  File::DirectIOFile closed_file;
+
+  std::latch do_reads{1};
+
+  EXPECT_TRUE(file.Seek(u16_data_offset, File::SeekOrigin::Begin));
+
+  // Concurrent access with copied handles works.
+  std::vector<std::thread> threads(thread_count);
+  for (auto& t : threads)
+  {
+    t = std::thread{[&do_reads, file, closed_file]() mutable {
+      EXPECT_FALSE(closed_file.IsOpen());  // a copied closed file is still closed
+
+      EXPECT_EQ(file.Tell(), u16_data_offset);  // current position is copied
+
+      std::array<u8, 1> one_byte{};
+
+      constexpr u64 small_offset = 3;
+
+      do_reads.wait();
+
+      EXPECT_TRUE(file.Seek(small_offset, File::SeekOrigin::Begin));
+      EXPECT_EQ(file.Tell(), small_offset);
+
+      // writes fail in read mode.
+      EXPECT_FALSE(file.Write(u8_test_data));
+      EXPECT_FALSE(file.OffsetWrite(0, u8_test_data.data(), 0));
+      EXPECT_EQ(file.Tell(), small_offset);
+
+      EXPECT_TRUE(file.Read(one_byte.data(), 0));  // read of zero succeeds.
+      EXPECT_EQ(file.Tell(), small_offset);        // unchanged position
+
+      // Reading at an explicit offset doesn't change the position
+      EXPECT_TRUE(file.OffsetRead(u8_test_data.size() - 1, one_byte));
+      EXPECT_EQ(file.Tell(), small_offset);
+      EXPECT_EQ(one_byte[0], u8_test_data.back());
+
+      EXPECT_EQ(file.GetSize(), final_file_size);
+      EXPECT_TRUE(file.Seek(-int(sizeof(u16_test_data)), File::SeekOrigin::End));
+
+      // We can't read beyond the end of the file.
+      EXPECT_FALSE(file.OffsetRead(big_offset, one_byte));
+      // A read of zero beyond the end works.
+      EXPECT_TRUE(file.OffsetRead(big_offset, one_byte.data(), 0));
+
+      // Reading the previously written data works.
+      std::array<u16, u16_test_data.size()> u16_buffer = {};
+      EXPECT_TRUE(file.Read(Common::AsWritableU8Span(u16_buffer)));
+      EXPECT_TRUE(std::ranges::equal(u16_buffer, u16_test_data));
+
+      // We can't read at the end of the file.
+      EXPECT_FALSE(file.Read(one_byte));
+      EXPECT_EQ(file.Tell(), file.GetSize());  // The position is unchanged.
+    }};
+  }
+
+  // We may close the file on our end before the other threads use it.
+  file.Close();
+
+  // ReadAndWrite does not truncate existing files.
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::ReadAndWrite));
+  EXPECT_EQ(file.GetSize(), final_file_size);
+  file.Close();
+
+  // Write doesn't truncate when the mode is changed.
+  EXPECT_TRUE(file.Open(m_file_path, File::AccessMode::Write, File::OpenMode::Existing));
+  EXPECT_EQ(file.GetSize(), final_file_size);
+
+  // Open a new handle to the same file.
+  File::DirectIOFile second_handle(m_file_path, File::AccessMode::Write, File::OpenMode::Always);
+  EXPECT_TRUE(second_handle.IsOpen());
+
+  const std::string destination_path_1 = m_file_path + ".dest_1";
+
+  // Rename through handle works when opened elsewhere.
+  EXPECT_TRUE(Rename(file, m_file_path, destination_path_1));
+  EXPECT_FALSE(File::Exists(m_file_path));
+  EXPECT_TRUE(File::Exists(destination_path_1));
+
+  const std::string destination_path_2 = m_file_path + ".dest_2";
+
+  // Note: Windows fails the next `Rename` if this file is kept open.
+  // I don't know if there is a nice way to make that work.
+  {
+    File::DirectIOFile another_file{destination_path_2, File::AccessMode::Write};
+    EXPECT_TRUE(another_file.IsOpen());
+  }
+
+  // Rename overwrites existing files.
+  EXPECT_TRUE(Rename(file, destination_path_1, destination_path_2));
+  EXPECT_FALSE(File::Exists(destination_path_1));
+  EXPECT_EQ(File::GetSize(destination_path_2), final_file_size);
+
+  const std::string destination_path_3 = m_file_path + ".dest_3";
+
+  // Truncate fails in Read mode.
+  File::Copy(destination_path_2, destination_path_3);
+  EXPECT_EQ(File::GetSize(destination_path_3), final_file_size);
+  {
+    File::DirectIOFile tmp{destination_path_3, File::AccessMode::Read, File::OpenMode::Truncate};
+    EXPECT_FALSE(tmp.IsOpen());
+    EXPECT_EQ(File::GetSize(destination_path_3), final_file_size);
+  }
+
+  // Truncate works with ReadAndWrite.
+  EXPECT_EQ(File::GetSize(destination_path_3), final_file_size);
+  {
+    File::DirectIOFile tmp{destination_path_3, File::AccessMode::ReadAndWrite,
+                           File::OpenMode::Truncate};
+    EXPECT_EQ(tmp.GetSize(), 0);
+    Delete(tmp, destination_path_3);
+  }
+
+  // Truncate works with Write.
+  File::Copy(destination_path_2, destination_path_3);
+  EXPECT_EQ(File::GetSize(destination_path_3), final_file_size);
+  {
+    File::DirectIOFile tmp{destination_path_3, File::AccessMode::Write, File::OpenMode::Truncate};
+    EXPECT_EQ(tmp.GetSize(), 0);
+    Delete(tmp, destination_path_3);
+  }
+
+  // Delete through handle works.
+  EXPECT_TRUE(Delete(file, destination_path_2));
+  EXPECT_FALSE(File::Exists(destination_path_2));
+
+  // The threads can read even after deleting everything.
+  do_reads.count_down();
+  std::ranges::for_each(threads, &std::thread::join);
+
+  file.Close();
+  EXPECT_TRUE(file.Open(destination_path_1, File::AccessMode::Read, File::OpenMode::Always));
+
+  // Required on Windows for the below to succeed.
+  second_handle.Close();
+
+  file.Close();
+  EXPECT_TRUE(file.Open(destination_path_2, File::AccessMode::Write, File::OpenMode::Always));
+}