diff --git a/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.Design.targets b/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.Design.targets
index a08b453e177d..5d9f5a2e0058 100644
--- a/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.Design.targets
+++ b/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.Design.targets
@@ -4,6 +4,7 @@
       $(CollectUpToDateCheckInputDesignTimeDependsOn);
       ResolveStaticWebAssetsConfiguration;
       ResolveProjectStaticWebAssets;
+      ResolveReferencedProjectsStaticWebAssetsConfiguration;
       CollectStaticWebAssetInputsDesignTime;
     </CollectUpToDateCheckInputDesignTimeDependsOn>
     <CollectUpToDateCheckOutputDesignTimeDependsOn>
@@ -61,6 +62,7 @@
 
     <ItemGroup>
       <UpToDateCheckOutput Include="$(StaticWebAssetBuildManifestPath)" Set="StaticWebAssets" />
+      <UpToDateCheckOutput Include="$(StaticWebAssetEndpointsBuildManifestPath)" Set="StaticWebAssets" />
     </ItemGroup>
 
   </Target>
diff --git a/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.References.targets b/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.References.targets
index 2ce47328997a..20537de45e73 100644
--- a/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.References.targets
+++ b/src/StaticWebAssetsSdk/Targets/Microsoft.NET.Sdk.StaticWebAssets.References.targets
@@ -46,14 +46,42 @@ Copyright (c) .NET Foundation. All rights reserved.
       <Output TaskParameter="TargetOutputs" ItemName="_ReferencedProjectsConfiguration" />
     </MSBuild>
 
+    <!-- During VS design-time builds (DesignTimeBuild=true), project references typically have BuildReference=false
+      so _StaticWebAssetProjectReference is empty and _ReferencedProjectsConfiguration is not populated.
+      To correctly populate the up-to-date check tracking file on initial project load (before any build
+      has occurred), we query referenced projects for their manifest paths directly. This is safe because
+      GetStaticWebAssetsProjectConfiguration only reads MSBuild properties and does not trigger a build.
+      The condition on _ReferencedProjectsConfiguration ensures this path only runs when the regular
+      build-time path produced no results, preventing duplicate entries. -->
+    <ItemGroup Condition="'$(BuildingInsideVisualStudio)' == 'true' and '$(DesignTimeBuild)' == 'true' and '@(_ReferencedProjectsConfiguration)' == '' and '@(ProjectReferenceWithConfiguration)' != ''">
+      <_StaticWebAssetDesignTimeProjectReference Include="@(_MSBuildProjectReferenceExistent)" />
+    </ItemGroup>
+
+    <MSBuild
+      Condition="'$(BuildingInsideVisualStudio)' == 'true' and '$(DesignTimeBuild)' == 'true' and '@(_StaticWebAssetDesignTimeProjectReference)' != ''"
+      Targets="GetStaticWebAssetsProjectConfiguration"
+      Properties="%(_StaticWebAssetDesignTimeProjectReference.SetConfiguration);%(_StaticWebAssetDesignTimeProjectReference.SetPlatform);%(_StaticWebAssetDesignTimeProjectReference.SetTargetFramework)"
+      RemoveProperties="%(_StaticWebAssetDesignTimeProjectReference.GlobalPropertiesToRemove);$(_GlobalPropertiesToRemoveFromProjectReferences)"
+      Projects="@(_StaticWebAssetDesignTimeProjectReference)"
+      BuildInParallel="$(BuildInParallel)"
+      SkipNonexistentTargets="true">
+
+      <Output TaskParameter="TargetOutputs" ItemName="_DesignTimeReferencedProjectsConfiguration" />
+    </MSBuild>
+
     <ItemGroup Condition="'$(BuildingInsideVisualStudio)' == 'true'">
+      <!-- From real builds (BuildReference=true path) -->
       <_ReferenceManifestPath Include="@(_ReferencedProjectsConfiguration->'%(BuildManifestPath)')" Condition="'%(_ReferencedProjectsConfiguration.BuildManifestPath)' != ''" />
+      <_ReferenceManifestPath Include="@(_ReferencedProjectsConfiguration->'%(EndpointsBuildManifestPath)')" Condition="'%(_ReferencedProjectsConfiguration.EndpointsBuildManifestPath)' != ''" />
+      <!-- From design-time builds (all references path, to fix timing bug on initial VS load) -->
+      <_ReferenceManifestPath Include="@(_DesignTimeReferencedProjectsConfiguration->'%(BuildManifestPath)')" Condition="'%(_DesignTimeReferencedProjectsConfiguration.BuildManifestPath)' != ''" />
+      <_ReferenceManifestPath Include="@(_DesignTimeReferencedProjectsConfiguration->'%(EndpointsBuildManifestPath)')" Condition="'%(_DesignTimeReferencedProjectsConfiguration.EndpointsBuildManifestPath)' != ''" />
     </ItemGroup>
 
     <WriteLinesToFile Condition="'$(BuildingInsideVisualStudio)' == 'true'"
       File="$(StaticWebAssetReferencesUpToDateCheckManifestPath)"
       Lines="@(_ReferenceManifestPath)"
-      Overwrite="false"
+      Overwrite="true"
       WriteOnlyWhenDifferent="true" />
 
     <MergeConfigurationProperties
@@ -97,6 +125,7 @@ Copyright (c) .NET Foundation. All rights reserved.
           <AdditionalPublishPropertiesToRemove>$(StaticWebAssetsAdditionalPublishPropertiesToRemove)</AdditionalPublishPropertiesToRemove>
           <!-- Build manifest -->
           <BuildManifestPath>$([System.IO.Path]::GetFullPath('$(StaticWebAssetBuildManifestPath)'))</BuildManifestPath>
+          <EndpointsBuildManifestPath>$([System.IO.Path]::GetFullPath('$(StaticWebAssetEndpointsBuildManifestPath)'))</EndpointsBuildManifestPath>
         </_StaticWebAssetThisProjectConfiguration>
       </ItemGroup>
   </Target>
diff --git a/test/Microsoft.NET.Sdk.StaticWebAssets.Tests/StaticWebAssetsDesignTimeTest.cs b/test/Microsoft.NET.Sdk.StaticWebAssets.Tests/StaticWebAssetsDesignTimeTest.cs
index 5b57ef2b2c53..e139ea06073f 100644
--- a/test/Microsoft.NET.Sdk.StaticWebAssets.Tests/StaticWebAssetsDesignTimeTest.cs
+++ b/test/Microsoft.NET.Sdk.StaticWebAssets.Tests/StaticWebAssetsDesignTimeTest.cs
@@ -51,8 +51,9 @@ public void CollectUpToDateCheckInputOutputsDesignTime_ReportsAddedFiles()
         var outputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCOutput.txt");
         new FileInfo(outputFilePath).Should().Exist();
         var outputFiles = File.ReadAllLines(outputFilePath);
-        outputFiles.Should().ContainSingle();
-        Path.GetFileName(outputFiles[0]).Should().Be("staticwebassets.build.json");
+        outputFiles.Should().HaveCount(2);
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.json");
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.endpoints.json");
     }
 
     [Fact]
@@ -86,8 +87,9 @@ public void CollectUpToDateCheckInputOutputsDesignTime_ReportsRemovedFiles_Once(
         var outputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCOutput.txt");
         new FileInfo(outputFilePath).Should().Exist();
         var outputFiles = File.ReadAllLines(outputFilePath);
-        outputFiles.Should().ContainSingle();
-        Path.GetFileName(outputFiles[0]).Should().Be("staticwebassets.build.json");
+        outputFiles.Should().HaveCount(2);
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.json");
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.endpoints.json");
     }
 
     [Fact]
@@ -105,7 +107,7 @@ public void CollectUpToDateCheckInputOutputsDesignTime_IncludesReferencedProject
         var msbuild = CreateMSBuildCommand(
             ProjectDirectory,
             "AppWithP2PReference",
-            "ResolveStaticWebAssetsConfiguration;ResolveProjectStaticWebAssets;CollectStaticWebAssetInputsDesignTime;CollectStaticWebAssetOutputsDesignTime");
+            "ResolveStaticWebAssetsConfiguration;ResolveProjectStaticWebAssets;ResolveReferencedProjectsStaticWebAssetsConfiguration;CollectStaticWebAssetInputsDesignTime;CollectStaticWebAssetOutputsDesignTime");
 
         msbuild.ExecuteWithoutRestore("/p:DesignTimeBuild=true", "/p:BuildingInsideVisualStudio=true", "/bl:design.binlog").Should().Pass();
 
@@ -113,14 +115,51 @@ public void CollectUpToDateCheckInputOutputsDesignTime_IncludesReferencedProject
         var inputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCInput.txt");
         new FileInfo(inputFilePath).Should().Exist();
         var inputFiles = File.ReadAllLines(inputFilePath);
-        inputFiles.Should().HaveCount(1);
+        inputFiles.Should().HaveCount(2);
+        inputFiles.Should().Contain(Path.Combine(ProjectDirectory.Path, "ClassLibrary", "obj", "Debug", DefaultTfm, "staticwebassets.build.json"));
+        inputFiles.Should().Contain(Path.Combine(ProjectDirectory.Path, "ClassLibrary", "obj", "Debug", DefaultTfm, "staticwebassets.build.endpoints.json"));
+
+        var outputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCOutput.txt");
+        new FileInfo(outputFilePath).Should().Exist();
+        var outputFiles = File.ReadAllLines(outputFilePath);
+        outputFiles.Should().HaveCount(2);
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.json");
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.endpoints.json");
+    }
+
+    [Fact]
+    public void CollectUpToDateCheckInputOutputsDesignTime_IncludesReferencedProjectsManifests_OnInitialLoad()
+    {
+        // This test verifies the timing bug fix: referenced project manifest paths must be available
+        // in the FUTDC inputs even before a full build has occurred (i.e., on initial VS load).
+        // Arrange
+        var testAsset = "RazorAppWithP2PReference";
+        ProjectDirectory = AddIntrospection(CreateAspNetSdkTestAsset(testAsset));
+
+        var build = CreateBuildCommand(ProjectDirectory, "AppWithP2PReference");
+
+        var msbuild = CreateMSBuildCommand(
+            ProjectDirectory,
+            "AppWithP2PReference",
+            "ResolveStaticWebAssetsConfiguration;ResolveProjectStaticWebAssets;ResolveReferencedProjectsStaticWebAssetsConfiguration;CollectStaticWebAssetInputsDesignTime;CollectStaticWebAssetOutputsDesignTime");
+
+        // Run design-time targets WITHOUT a prior full build to simulate initial VS project load
+        msbuild.ExecuteWithoutRestore("/p:DesignTimeBuild=true", "/p:BuildingInsideVisualStudio=true", "/bl:design.binlog").Should().Pass();
+
+        // The referenced project manifest paths must be tracked as inputs, even without a prior build
+        var inputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCInput.txt");
+        new FileInfo(inputFilePath).Should().Exist();
+        var inputFiles = File.ReadAllLines(inputFilePath);
+        inputFiles.Should().HaveCount(2);
         inputFiles.Should().Contain(Path.Combine(ProjectDirectory.Path, "ClassLibrary", "obj", "Debug", DefaultTfm, "staticwebassets.build.json"));
+        inputFiles.Should().Contain(Path.Combine(ProjectDirectory.Path, "ClassLibrary", "obj", "Debug", DefaultTfm, "staticwebassets.build.endpoints.json"));
 
         var outputFilePath = Path.Combine(build.GetIntermediateDirectory().FullName, "StaticWebAssetsUTDCOutput.txt");
         new FileInfo(outputFilePath).Should().Exist();
         var outputFiles = File.ReadAllLines(outputFilePath);
-        outputFiles.Should().ContainSingle();
-        Path.GetFileName(outputFiles[0]).Should().Be("staticwebassets.build.json");
+        outputFiles.Should().HaveCount(2);
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.json");
+        outputFiles.Should().Contain(x => Path.GetFileName(x) == "staticwebassets.build.endpoints.json");
     }
 
     private static MSBuildCommand CreateMSBuildCommand(TestAsset testAsset, string relativeProjectPath, string targets)