diff --git a/documentation/general/dotnet-run-file.md b/documentation/general/dotnet-run-file.md
index 49a4946936d5..fff05c0734b3 100644
--- a/documentation/general/dotnet-run-file.md
+++ b/documentation/general/dotnet-run-file.md
@@ -267,8 +267,9 @@ We do not limit these directives to appear only in entry point files because it
 - which also makes it possible to share it independently or symlink it to multiple script folders,
 - and it's similar to `global using`s which users usually put into a single file but don't have to.
 
-We disallow duplicate `#:` directives to allow us design some deduplication mechanism in the future.
+We disallow duplicate `#:` directives (except `#:project` and `#:ref`) to allow us to design some deduplication mechanism in the future.
 Specifically, directives are considered duplicate if their type and name (case insensitive) are equal.
+`#:project` and `#:ref` duplicates are allowed because MSBuild allows duplicate `<ProjectReference />` items.
 Later with deduplication, separate "self-contained" utilities could reference overlapping sets of packages
 even if they end up in the same compilation.
 For example, properties could be concatenated via `;`, more specific package versions could override less specific ones.
diff --git a/src/Cli/Microsoft.DotNet.FileBasedPrograms/FileLevelDirectiveHelpers.cs b/src/Cli/Microsoft.DotNet.FileBasedPrograms/FileLevelDirectiveHelpers.cs
index 2303d48b4c2e..711cb07fb8fb 100644
--- a/src/Cli/Microsoft.DotNet.FileBasedPrograms/FileLevelDirectiveHelpers.cs
+++ b/src/Cli/Microsoft.DotNet.FileBasedPrograms/FileLevelDirectiveHelpers.cs
@@ -156,15 +156,19 @@ public static void FindLeadingDirectives(
 
                 if (CSharpDirective.Parse(context) is { } directive)
                 {
-                    // If the directive is already present, report an error.
-                    if (deduplicated.TryGetValue(directive, out var existingDirective))
+                    // Duplicate #:project and #:ref directives are allowed (MSBuild can handle that).
+                    if (directive is not (CSharpDirective.Project or CSharpDirective.Ref))
                     {
-                        var typeAndName = $"#:{existingDirective.GetType().Name.ToLowerInvariant()} {existingDirective.Name}";
-                        context.ReportError(directive.Info.Span, string.Format(FileBasedProgramsResources.DuplicateDirective, typeAndName));
-                    }
-                    else
-                    {
-                        deduplicated.Add(directive, directive);
+                        // If the directive is already present, report an error.
+                        if (deduplicated.TryGetValue(directive, out var existingDirective))
+                        {
+                            var typeAndName = $"#:{existingDirective.GetType().Name.ToLowerInvariant()} {existingDirective.Name}";
+                            context.ReportError(directive.Info.Span, string.Format(FileBasedProgramsResources.DuplicateDirective, typeAndName));
+                        }
+                        else
+                        {
+                            deduplicated.Add(directive, directive);
+                        }
                     }
 
                     builder?.Add(directive);
diff --git a/test/dotnet.Tests/CommandTests/Run/RunFileTests_Directives.cs b/test/dotnet.Tests/CommandTests/Run/RunFileTests_Directives.cs
index e4f228613be1..4d28b6ac08af 100644
--- a/test/dotnet.Tests/CommandTests/Run/RunFileTests_Directives.cs
+++ b/test/dotnet.Tests/CommandTests/Run/RunFileTests_Directives.cs
@@ -276,6 +276,7 @@ public void ProjectReference_Duplicate(string? subdir)
             </Project>
             """);
 
+        // Duplicate #:project directives are allowed (MSBuild can handle that).
         File.WriteAllText(filePath, """
             #:project dir/
             #:project dir/
@@ -285,8 +286,8 @@ public void ProjectReference_Duplicate(string? subdir)
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()
-            .Should().Fail()
-            .And.HaveStdErrContaining(DirectiveError(filePath, 2, FileBasedProgramsResources.DuplicateDirective, "#:project dir/"));
+            .Should().Pass()
+            .And.HaveStdOut("Hello");
 
         File.WriteAllText(filePath, """
             #:project dir/
@@ -294,7 +295,6 @@ public void ProjectReference_Duplicate(string? subdir)
             Console.WriteLine("Hello");
             """);
 
-        // https://github.com/dotnet/sdk/issues/51139: we should detect the duplicate project reference
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()
@@ -307,7 +307,6 @@ public void ProjectReference_Duplicate(string? subdir)
             Console.WriteLine("Hello");
             """);
 
-        // https://github.com/dotnet/sdk/issues/51139: we should detect the duplicate project reference
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()
@@ -574,6 +573,7 @@ public static class Greeter
             }
             """);
 
+        // Duplicate #:ref directives are allowed (MSBuild can handle that).
         File.WriteAllText(filePath, """
             #:ref lib.cs
             #:ref lib.cs
@@ -583,8 +583,8 @@ public static class Greeter
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()
-            .Should().Fail()
-            .And.HaveStdErrContaining(DirectiveError(filePath, 2, FileBasedProgramsResources.DuplicateDirective, "#:ref lib.cs"));
+            .Should().Pass()
+            .And.HaveStdOut("Hello!");
 
         File.WriteAllText(filePath, """
             #:ref lib.cs
@@ -592,7 +592,6 @@ public static class Greeter
             Console.WriteLine(MyLib.Greeter.Greet());
             """);
 
-        // https://github.com/dotnet/sdk/issues/51139: we should detect the duplicate ref
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()
@@ -605,7 +604,6 @@ public static class Greeter
             Console.WriteLine(MyLib.Greeter.Greet());
             """);
 
-        // https://github.com/dotnet/sdk/issues/51139: we should detect the duplicate ref
         new DotnetCommand(Log, "run", relativeFilePath)
             .WithWorkingDirectory(testInstance.Path)
             .Execute()