diff --git a/localization/strings/en-US/Resources.resw b/localization/strings/en-US/Resources.resw
index 55a700b83..68c7e08b7 100644
--- a/localization/strings/en-US/Resources.resw
+++ b/localization/strings/en-US/Resources.resw
@@ -853,6 +853,10 @@ For information please visit https://aka.ms/wslinstall</value>
     <value>Failed to create the swap disk in '{}': {}</value>
     <comment>{FixedPlaceholder="{}"}Command line arguments, file names and string inserts should not be translated</comment>
   </data>
+  <data name="MessageSwapFileConflictsWithDistroVhd" xml:space="preserve">
+    <value>The swap file path '{}' specified in .wslconfig conflicts with the data disk for distribution '{}'. Using a distribution's data disk as swap will destroy its contents. Please change the 'swapFile' setting in .wslconfig to a different path.</value>
+    <comment>{FixedPlaceholder="{}"}{Locked=".wslconfig"}{Locked="swapFile"}Command line arguments, file names and string inserts should not be translated</comment>
+  </data>
   <data name="MessageNestedVirtualizationNotSupported" xml:space="preserve">
     <value>Nested virtualization is not supported on this machine.</value>
   </data>
diff --git a/src/windows/common/wslutil.cpp b/src/windows/common/wslutil.cpp
index 421caf89e..c42079a87 100644
--- a/src/windows/common/wslutil.cpp
+++ b/src/windows/common/wslutil.cpp
@@ -85,6 +85,7 @@ static const std::map<HRESULT, LPCWSTR> g_commonErrors{
     X(WSL_E_DISTRIBUTION_NAME_NEEDED),
     X(WSL_E_INVALID_JSON),
     X(WSL_E_VM_CRASHED),
+    X(WSL_E_SWAP_FILE_CONFLICTS_WITH_DISTRO),
     X(WSL_E_NOT_A_LINUX_DISTRO),
     X(E_ACCESSDENIED),
     X_WIN32(ERROR_NOT_FOUND),
diff --git a/src/windows/service/exe/LxssUserSession.cpp b/src/windows/service/exe/LxssUserSession.cpp
index 2ad6469c9..5c0dab8e3 100644
--- a/src/windows/service/exe/LxssUserSession.cpp
+++ b/src/windows/service/exe/LxssUserSession.cpp
@@ -2829,6 +2829,56 @@ void LxssUserSessionImpl::_CreateVm()
         const auto userToken = wsl::windows::common::security::GetUserToken(TokenImpersonation);
         auto config = _GetResultantConfig(userToken.get());
 
+        // Validate that the swap file path does not point to any distribution's data VHD.
+        // Using a distribution's VHD as swap would destroy its filesystem with mkswap.
+        if (!config.SwapFilePath.empty())
+        {
+            auto swapFilePath = config.SwapFilePath;
+            if (!wsl::windows::common::string::IsPathComponentEqual(swapFilePath.extension().native(), wsl::windows::common::wslutil::c_vhdxFileExtension))
+            {
+                swapFilePath += wsl::windows::common::wslutil::c_vhdxFileExtension;
+            }
+
+            std::error_code error;
+            auto canonicalSwapPath = std::filesystem::weakly_canonical(swapFilePath, error);
+            if (error)
+            {
+                LOG_WIN32(error.value());
+                canonicalSwapPath = std::move(swapFilePath);
+            }
+
+            const wil::unique_hkey lxssKey = s_OpenLxssUserKey();
+            for (const auto& distro : _EnumerateDistributions(lxssKey.get()))
+            {
+                std::filesystem::path distroVhdPath;
+                try
+                {
+                    distroVhdPath = distro.ReadVhdFilePath();
+                }
+                catch (...)
+                {
+                    LOG_CAUGHT_EXCEPTION();
+                    // skip distro whose registration is broken
+                    continue;
+                }
+
+                auto canonicalDistroPath = std::filesystem::weakly_canonical(distroVhdPath, error);
+                if (error)
+                {
+                    LOG_WIN32(error.value());
+                    canonicalDistroPath = std::move(distroVhdPath);
+                }
+
+                if (wsl::windows::common::string::IsPathComponentEqual(canonicalSwapPath.native(), canonicalDistroPath.native()))
+                {
+                    auto distroName = distro.Read(Property::Name);
+                    THROW_HR_WITH_USER_ERROR(
+                        WSL_E_SWAP_FILE_CONFLICTS_WITH_DISTRO,
+                        wsl::shared::Localization::MessageSwapFileConflictsWithDistroVhd(canonicalSwapPath.c_str(), distroName.c_str()));
+                }
+            }
+        }
+
         // Initialize policies for the plugin interface.
         WSLVmCreationSettings userSettings{};
         WI_SetFlagIf(userSettings.CustomConfigurationFlags, WSLUserConfigurationCustomKernel, !config.KernelPath.empty());
diff --git a/src/windows/service/inc/wslservice.idl b/src/windows/service/inc/wslservice.idl
index c68ad7567..bc0613266 100644
--- a/src/windows/service/inc/wslservice.idl
+++ b/src/windows/service/inc/wslservice.idl
@@ -394,3 +394,4 @@ cpp_quote("#define WSL_E_DISK_CORRUPTED MAKE_HRESULT(SEVERITY_ERROR, FACILITY_IT
 cpp_quote("#define WSL_E_DISTRIBUTION_NAME_NEEDED MAKE_HRESULT(SEVERITY_ERROR, FACILITY_ITF, WSL_E_BASE + 0x30) /* 0x80040330 */")
 cpp_quote("#define WSL_E_INVALID_JSON MAKE_HRESULT(SEVERITY_ERROR, FACILITY_ITF, WSL_E_BASE + 0x31) /* 0x80040331 */")
 cpp_quote("#define WSL_E_VM_CRASHED MAKE_HRESULT(SEVERITY_ERROR, FACILITY_ITF, WSL_E_BASE + 0x32) /* 0x80040332 */")
+cpp_quote("#define WSL_E_SWAP_FILE_CONFLICTS_WITH_DISTRO MAKE_HRESULT(SEVERITY_ERROR, FACILITY_ITF, WSL_E_BASE + 0x33) /* 0x80040333 */")
diff --git a/test/windows/UnitTests.cpp b/test/windows/UnitTests.cpp
index 8d5e6b39f..654850380 100644
--- a/test/windows/UnitTests.cpp
+++ b/test/windows/UnitTests.cpp
@@ -1798,6 +1798,28 @@ Error code: Wsl/InstallDistro/WSL_E_DISTRO_NOT_FOUND
         validateSwapSize(L"200M");
     }
 
+    TEST_METHOD(SwapFileConflictsWithDistroVhd)
+    {
+        WSL2_TEST_ONLY();
+
+        // Read the test distro's VHD path from the registry.
+        auto distroKey = OpenDistributionKey(LXSS_DISTRO_NAME_TEST_L);
+        auto basePath = wsl::windows::common::registry::ReadString(distroKey.get(), nullptr, L"BasePath", L"");
+        auto vhdFileName = wsl::windows::common::registry::ReadString(distroKey.get(), nullptr, L"VhdFileName", L"ext4.vhdx");
+        auto vhdPath = std::filesystem::path(basePath) / vhdFileName;
+
+        // Set swapFile to point to the distro's data VHD.
+        // Escape backslashes for .wslconfig ini parsing.
+        auto swapFileConfig = std::regex_replace(vhdPath.wstring(), std::wregex(L"\\\\"), L"\\\\");
+        WslConfigChange configChange(LxssGenerateTestConfig() + L"\nswap=256MB\nswapFile=" + swapFileConfig);
+
+        // Launching the distro should fail because swapFile conflicts with the distro's VHD.
+        auto [output, _] = LxsstuLaunchWslAndCaptureOutput(L"echo ok", -1);
+
+        // Verify the error contains the expected error code.
+        VERIFY_IS_TRUE(output.find(L"WSL_E_SWAP_FILE_CONFLICTS_WITH_DISTRO") != std::wstring::npos);
+    }
+
     TEST_METHOD(InitDoesntBlockSignals)
     {
         auto [output, _] = LxsstuLaunchWslAndCaptureOutput(L"grep -iF SigBlk < /proc/1/status");