diff --git a/src/Cli/dotnet/Commands/Run/RunCommand.cs b/src/Cli/dotnet/Commands/Run/RunCommand.cs
index 542fc76ffbcd..9c11228ab213 100644
--- a/src/Cli/dotnet/Commands/Run/RunCommand.cs
+++ b/src/Cli/dotnet/Commands/Run/RunCommand.cs
@@ -538,6 +538,15 @@ internal static void ThrowUnableToRunError(ProjectInstance project)
             projectFileOrDirectoryPath = Directory.GetCurrentDirectory();
         }
 
+        // Normalize path separators to handle Windows-style paths on non-Windows platforms.
+        // This is supported for backward compatibility in 'dotnet run' only, not for all CLI commands.
+        // Converting backslashes to forward slashes allows PowerShell scripts using Windows-style paths
+        // to work cross-platform, maintaining compatibility with .NET 9 behavior.
+        if (Path.DirectorySeparatorChar != '\\')
+        {
+            projectFileOrDirectoryPath = projectFileOrDirectoryPath.Replace('\\', '/');
+        }
+
         string? projectFilePath = Directory.Exists(projectFileOrDirectoryPath)
             ? TryFindSingleProjectInDirectory(projectFileOrDirectoryPath)
             : projectFileOrDirectoryPath;
diff --git a/test/dotnet.Tests/CommandTests/Run/RunParserTests.cs b/test/dotnet.Tests/CommandTests/Run/RunParserTests.cs
index 3c2897bbe34e..b47f27a41e5a 100644
--- a/test/dotnet.Tests/CommandTests/Run/RunParserTests.cs
+++ b/test/dotnet.Tests/CommandTests/Run/RunParserTests.cs
@@ -27,5 +27,35 @@ public void RunParserCanGetArgumentFromDoubleDash()
             var runCommand = RunCommand.FromArgs(new[] { "--project", projectPath, "--", "foo" });
             runCommand.ApplicationArgs.Single().Should().Be("foo");
         }
+
+        [WindowsOnlyFact]
+        public void RunParserAcceptsWindowsPathSeparatorsOnWindows()
+        {
+            var tam = new TestAssetsManager(output);
+            var testAsset = tam.CopyTestAsset("HelloWorld").WithSource();
+            var newWorkingDir = testAsset.Path;
+
+            Directory.SetCurrentDirectory(newWorkingDir);
+            var projectPath = @".\HelloWorld.csproj";
+                
+            // Should not throw on Windows
+            var runCommand = RunCommand.FromArgs(new[] { "--project", projectPath });
+            runCommand.ProjectFileFullPath.Should().NotBeNull();
+        }
+
+        [UnixOnlyFact]
+        public void RunParserAcceptsWindowsPathSeparatorsOnLinux()
+        {
+            var tam = new TestAssetsManager(output);
+            var testAsset = tam.CopyTestAsset("HelloWorld").WithSource();
+            var newWorkingDir = testAsset.Path;
+
+            Directory.SetCurrentDirectory(newWorkingDir);
+            var projectPath = @".\HelloWorld.csproj";
+                
+            // Should not throw on Linux with backslash separators
+            var runCommand = RunCommand.FromArgs(new[] { "--project", projectPath });
+            runCommand.ProjectFileFullPath.Should().NotBeNull();
+        }
     }
 }