diff --git a/src/LanguageServer/Microsoft.CodeAnalysis.LanguageServer/HostWorkspace/VirtualProject.cs b/src/LanguageServer/Microsoft.CodeAnalysis.LanguageServer/HostWorkspace/VirtualProject.cs
index e2cd47a2169f2..8bada428d0f98 100644
--- a/src/LanguageServer/Microsoft.CodeAnalysis.LanguageServer/HostWorkspace/VirtualProject.cs
+++ b/src/LanguageServer/Microsoft.CodeAnalysis.LanguageServer/HostWorkspace/VirtualProject.cs
@@ -2,7 +2,10 @@
 // The .NET Foundation licenses this file to you under the MIT license.
 // See the LICENSE file in the project root for more information.
 
+using System.Runtime.InteropServices;
 using System.Security;
+using System.Security.Cryptography;
+using System.Text;
 using Microsoft.CodeAnalysis.CSharp;
 using Microsoft.CodeAnalysis.Text;
 using Roslyn.Utilities;
@@ -21,6 +24,45 @@ internal static class VirtualCSharpFileBasedProgramProject
     internal static string GetVirtualProjectPath(string documentFilePath)
         => Path.ChangeExtension(documentFilePath, ".csproj");
 
+    #region TODO: Copy-pasted from dotnet run-api. Delete when run-api is adopted.
+    // See https://github.com/dotnet/sdk/blob/b5dbc69cc28676ac6ea615654c8016a11b75e747/src/Cli/Microsoft.DotNet.Cli.Utils/Sha256Hasher.cs#L10
+    private static class Sha256Hasher
+    {
+        public static string Hash(string text)
+        {
+            byte[] bytes = Encoding.UTF8.GetBytes(text);
+            byte[] hash = SHA256.HashData(bytes);
+#if NET9_0_OR_GREATER
+            return Convert.ToHexStringLower(hash);
+#else
+            return Convert.ToHexString(hash).ToLowerInvariant();
+#endif
+        }
+
+        public static string HashWithNormalizedCasing(string text)
+        {
+            return Hash(text.ToUpperInvariant());
+        }
+    }
+
+    // TODO: this is a copy of SDK run-api code. Must delete when adopting run-api.
+    // See https://github.com/dotnet/sdk/blob/5a4292947487a9d34f4256c1d17fb3dc26859174/src/Cli/dotnet/Commands/Run/VirtualProjectBuildingCommand.cs#L449
+    internal static string GetArtifactsPath(string entryPointFileFullPath)
+    {
+        // We want a location where permissions are expected to be restricted to the current user.
+        string directory = RuntimeInformation.IsOSPlatform(OSPlatform.Windows)
+            ? Path.GetTempPath()
+            : Environment.GetFolderPath(Environment.SpecialFolder.LocalApplicationData);
+
+        // Include entry point file name so the directory name is not completely opaque.
+        string fileName = Path.GetFileNameWithoutExtension(entryPointFileFullPath);
+        string hash = Sha256Hasher.HashWithNormalizedCasing(entryPointFileFullPath);
+        string directoryName = $"{fileName}-{hash}";
+
+        return Path.Join(directory, "dotnet", "runfile", directoryName);
+    }
+    #endregion
+
     internal static (string virtualProjectXml, bool isFileBasedProgram) MakeVirtualProjectContent(string documentFilePath, SourceText text)
     {
         Contract.ThrowIfFalse(PathUtilities.IsAbsolute(documentFilePath));
@@ -30,48 +72,74 @@ internal static (string virtualProjectXml, bool isFileBasedProgram) MakeVirtualP
         var root = tree.GetRoot();
         var isFileBasedProgram = root.GetLeadingTrivia().Any(SyntaxKind.IgnoredDirectiveTrivia) || root.ChildNodes().Any(node => node.IsKind(SyntaxKind.GlobalStatement));
 
+        var artifactsPath = GetArtifactsPath(documentFilePath);
+
+        var targetFramework = Environment.GetEnvironmentVariable("DOTNET_RUN_FILE_TFM") ?? "net10.0";
+
         var virtualProjectXml = $"""
-            <Project Sdk="Microsoft.NET.Sdk">
+            <Project>
+
+              <PropertyGroup>
+                <IncludeProjectNameInArtifactsPaths>false</IncludeProjectNameInArtifactsPaths>
+                <ArtifactsPath>{SecurityElement.Escape(artifactsPath)}</ArtifactsPath>
+              </PropertyGroup>
 
-                <PropertyGroup>
-                    <OutputType>Exe</OutputType>
-                    <TargetFramework>net8.0</TargetFramework>
-                    <ImplicitUsings>enable</ImplicitUsings>
-                    <Nullable>enable</Nullable>
-                    <Features>$(Features);FileBasedProgram</Features>
-                    <EnableDefaultCompileItems>false</EnableDefaultCompileItems>
-                </PropertyGroup>
+              <!-- We need to explicitly import Sdk props/targets so we can override the targets below. -->
+              <Import Project="Sdk.props" Sdk="Microsoft.NET.Sdk" />
 
+              <PropertyGroup>
+                <OutputType>Exe</OutputType>
+                <TargetFramework>{SecurityElement.Escape(targetFramework)}</TargetFramework>
+                <ImplicitUsings>enable</ImplicitUsings>
+                <Nullable>enable</Nullable>
+              </PropertyGroup>
+
+              <PropertyGroup>
+                <EnableDefaultItems>false</EnableDefaultItems>
+              </PropertyGroup>
+
+              <PropertyGroup>
+                <LangVersion>preview</LangVersion>
+              </PropertyGroup>
+
+              <PropertyGroup>
+                <Features>$(Features);FileBasedProgram</Features>
+              </PropertyGroup>
+
+
+              <ItemGroup>
+                <Compile Include="{SecurityElement.Escape(documentFilePath)}" />
+              </ItemGroup>
+
+              <Import Project="Sdk.targets" Sdk="Microsoft.NET.Sdk" />
+
+              <!--
+                Override targets which don't work with project files that are not present on disk.
+                See https://github.com/NuGet/Home/issues/14148.
+              -->
+
+              <Target Name="_FilterRestoreGraphProjectInputItems"
+                      DependsOnTargets="_LoadRestoreGraphEntryPoints"
+                      Returns="@(FilteredRestoreGraphProjectInputItems)">
+                <ItemGroup>
+                  <FilteredRestoreGraphProjectInputItems Include="@(RestoreGraphProjectInputItems)" />
+                </ItemGroup>
+              </Target>
+
+              <Target Name="_GetAllRestoreProjectPathItems"
+                      DependsOnTargets="_FilterRestoreGraphProjectInputItems"
+                      Returns="@(_RestoreProjectPathItems)">
                 <ItemGroup>
-                    <Compile Include="{SecurityElement.Escape(documentFilePath)}" />
+                  <_RestoreProjectPathItems Include="@(FilteredRestoreGraphProjectInputItems)" />
                 </ItemGroup>
+              </Target>
+
+              <Target Name="_GenerateRestoreGraph"
+                      DependsOnTargets="_FilterRestoreGraphProjectInputItems;_GetAllRestoreProjectPathItems;_GenerateRestoreGraphProjectEntry;_GenerateProjectRestoreGraph"
+                      Returns="@(_RestoreGraphEntry)">
+                <!-- Output from dependency _GenerateRestoreGraphProjectEntry and _GenerateProjectRestoreGraph -->
+              </Target>
 
-                <!--
-                  Override targets which don't work with project files that are not present on disk.
-                  See https://github.com/NuGet/Home/issues/14148.
-                -->
-
-                <Target Name="_FilterRestoreGraphProjectInputItems"
-                        DependsOnTargets="_LoadRestoreGraphEntryPoints"
-                        Returns="@(FilteredRestoreGraphProjectInputItems)">
-                  <ItemGroup>
-                    <FilteredRestoreGraphProjectInputItems Include="@(RestoreGraphProjectInputItems)" />
-                  </ItemGroup>
-                </Target>
-
-                <Target Name="_GetAllRestoreProjectPathItems"
-                        DependsOnTargets="_FilterRestoreGraphProjectInputItems"
-                        Returns="@(_RestoreProjectPathItems)">
-                  <ItemGroup>
-                    <_RestoreProjectPathItems Include="@(FilteredRestoreGraphProjectInputItems)" />
-                  </ItemGroup>
-                </Target>
-
-                <Target Name="_GenerateRestoreGraph"
-                        DependsOnTargets="_FilterRestoreGraphProjectInputItems;_GetAllRestoreProjectPathItems;_GenerateRestoreGraphProjectEntry;_GenerateProjectRestoreGraph"
-                        Returns="@(_RestoreGraphEntry)">
-                  <!-- Output from dependency _GenerateRestoreGraphProjectEntry and _GenerateProjectRestoreGraph -->
-                </Target>
             </Project>
             """;