diff --git a/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets b/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
index 707ce66956448e..01d02adbc23fc8 100644
--- a/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
+++ b/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
@@ -349,7 +349,6 @@ Copyright (c) .NET Foundation. All rights reserved.
     <PropertyGroup>
       <_WasmBuildWebCilPath>$([MSBuild]::NormalizeDirectory($(IntermediateOutputPath), 'webcil'))</_WasmBuildWebCilPath>
       <_WasmBuildTmpWebCilPath>$([MSBuild]::NormalizeDirectory($(IntermediateOutputPath), 'tmp-webcil'))</_WasmBuildTmpWebCilPath>
-      <_WasmBuildOuputPath>$([MSBuild]::NormalizeDirectory('$(OutputPath)', 'wwwroot'))</_WasmBuildOuputPath>
     </PropertyGroup>
 
     <ConvertDllsToWebCil Candidates="@(_BuildAssetsCandidates)" IntermediateOutputPath="$(_WasmBuildTmpWebCilPath)" OutputPath="$(_WasmBuildWebCilPath)" IsEnabled="$(_WasmEnableWebcil)">
@@ -358,6 +357,8 @@ Copyright (c) .NET Foundation. All rights reserved.
     </ConvertDllsToWebCil>
 
     <ItemGroup>
+      <!-- Set per-item ContentRoot so each asset's Identity matches its actual file on disk -->
+      <_WebCilAssetsCandidates Update="@(_WebCilAssetsCandidates)" ContentRoot="%(RootDir)%(Directory)" />
       <_WasmFingerprintPatterns Include="WasmFiles" Pattern="*.wasm" Expression="#[.{fingerprint}]!" />
       <_WasmFingerprintPatterns Include="DllFiles" Pattern="*.dll" Expression="#[.{fingerprint}]!" />
       <_WasmFingerprintPatterns Include="DatFiles" Pattern="*.dat" Expression="#[.{fingerprint}]!" />
@@ -372,7 +373,6 @@ Copyright (c) .NET Foundation. All rights reserved.
       AssetRole="Primary"
       CopyToOutputDirectory="PreserveNewest"
       CopyToPublishDirectory="Never"
-      ContentRoot="$(_WasmBuildOuputPath)"
       FingerprintCandidates="$(_WasmFingerprintAssets)"
       FingerprintPatterns="@(FingerprintPatterns);@(_WasmFingerprintPatterns)"
       BasePath="$(StaticWebAssetBasePath)"
@@ -518,7 +518,7 @@ Copyright (c) .NET Foundation. All rights reserved.
       AssetTraitValue="manifest"
       CopyToOutputDirectory="PreserveNewest"
       CopyToPublishDirectory="Never"
-      ContentRoot="$(OutDir)wwwroot"
+      ContentRoot="$(IntermediateOutputPath)"
       BasePath="$(StaticWebAssetBasePath)"
     >
       <Output TaskParameter="Assets" ItemName="_WasmBuildBootConfigStaticWebAsset" />
@@ -584,18 +584,10 @@ Copyright (c) .NET Foundation. All rights reserved.
   </Target>
 
   <Target Name="_AddWasmPreloadBuildProperties" DependsOnTargets="_WasmConfigurePreload;_AddWasmStaticWebAssets" BeforeTargets="GenerateStaticWebAssetsManifest" Condition="'$(_WasmPreloadAssets)' == 'true'">
-    <PropertyGroup>
-      <_WasmBootConfigFileNameWithoutExtension>$([System.IO.Path]::GetFileNameWithoutExtension('$(_WasmBootConfigFileName)'))</_WasmBootConfigFileNameWithoutExtension>
-      <_WasmBootConfigFileExtension>$([System.IO.Path]::GetExtension('$(_WasmBootConfigFileName)'))</_WasmBootConfigFileExtension>
-    </PropertyGroup>
-    <ItemGroup>
-      <_WasmPreloadBuildScriptAsset Include="@(StaticWebAsset)" Condition="'$(_WasmFingerprintAssets)' == 'true' and '$(_WasmFingerprintBootConfig)' == 'true' and '%(AssetKind)' != 'Publish' and '%(FileName)%(Extension)' == '$(_WasmBootConfigFileNameWithoutExtension).%(Fingerprint)$(_WasmBootConfigFileExtension)'" />
-      <_WasmPreloadBuildScriptAsset Include="@(StaticWebAsset)" Condition="('$(_WasmFingerprintAssets)' != 'true' or '$(_WasmFingerprintBootConfig)' != 'true') and '%(AssetKind)' != 'Publish' and '%(FileName)%(Extension)' == '$(_WasmBootConfigFileName)'" />
-    </ItemGroup>
 
     <FilterStaticWebAssetEndpoints
       Endpoints="@(StaticWebAssetEndpoint)"
-      Assets="@(_WasmPreloadBuildScriptAsset)"
+      Assets="@(_WasmBuildBootConfigStaticWebAsset)"
       Filters="@(_WasmPreloadEndpointFilter)"
     >
       <Output TaskParameter="FilteredEndpoints" ItemName="_WasmPreloadBuildScriptAssetEndpoint" />
@@ -614,13 +606,10 @@ Copyright (c) .NET Foundation. All rights reserved.
     </ItemGroup>
   </Target>
   <Target Name="_AddWasmPreloadPublishProperties" DependsOnTargets="_WasmConfigurePreload;_AddPublishWasmBootJsonToStaticWebAssets" BeforeTargets="GenerateStaticWebAssetsPublishManifest" Condition="'$(_WasmPreloadAssets)' == 'true'">
-    <ItemGroup>
-      <_WasmPreloadPublishScriptAsset Include="@(StaticWebAsset)" Condition="'%(AssetKind)' != 'Build' and '%(FileName)%(Extension)' == '$(_WasmPublishBootConfigFileName)'" />
-    </ItemGroup>
 
     <FilterStaticWebAssetEndpoints
       Endpoints="@(StaticWebAssetEndpoint)"
-      Assets="@(_WasmPreloadPublishScriptAsset)"
+      Assets="@(_WasmPublishBootConfigStaticWebAsset)"
       Filters="@(_WasmPreloadEndpointFilter)"
     >
       <Output TaskParameter="FilteredEndpoints" ItemName="_WasmPreloadPublishScriptAssetEndpoint" />
@@ -729,6 +718,18 @@ Copyright (c) .NET Foundation. All rights reserved.
       <_NewWebCilPublishStaticWebAssetsCandidatesNoMetadata
         Include="@(_NewWebCilPublishStaticWebAssetsCandidates)"
         RemoveMetadata="Integrity;Fingerprint" />
+      <!-- Set per-item ContentRoot so each asset's Identity matches its actual file on disk.
+           Clear stale Fingerprint/Integrity so DefineStaticWebAssets recomputes from the actual file. -->
+      <_NewWebCilPublishStaticWebAssetsCandidatesNoMetadata Update="@(_NewWebCilPublishStaticWebAssetsCandidatesNoMetadata)" ContentRoot="%(RootDir)%(Directory)" />
+      <_PromotedWasmPublishStaticWebAssets Update="@(_PromotedWasmPublishStaticWebAssets)" ContentRoot="%(RootDir)%(Directory)" Fingerprint="" Integrity="" />
+      <!-- Satellite (Culture) promoted assets are Related assets whose RelatedAsset points to a build-time path
+           that doesn't match any publish-time candidate. Promote them to Primary so DefineStaticWebAssets
+           processes them as standalone assets instead of trying to match a parent. -->
+      <_PromotedWasmPublishStaticWebAssets
+        Update="@(_PromotedWasmPublishStaticWebAssets)"
+        Condition="'%(_PromotedWasmPublishStaticWebAssets.AssetTraitName)' == 'Culture'"
+        AssetRole="Primary"
+        RelatedAsset="" />
     </ItemGroup>
 
     <DefineStaticWebAssets CandidateAssets="@(_NewWebCilPublishStaticWebAssetsCandidatesNoMetadata);@(_PromotedWasmPublishStaticWebAssets)">
diff --git a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmPublishAssets.cs b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmPublishAssets.cs
index 69205e6f3b982f..dfa1bce752144f 100644
--- a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmPublishAssets.cs
+++ b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmPublishAssets.cs
@@ -332,23 +332,11 @@ static bool IsDotNetWasm(string key)
 
     private TaskItem CreatePromotedAsset(ITaskItem asset)
     {
-        string newAssetItemSpec = asset.ItemSpec;
-        string newAssetRelativePath = asset.GetMetadata("RelativePath");
-
-        if (FingerprintAssets)
-        {
-            string assetDirectory = Path.GetDirectoryName(asset.ItemSpec);
-            string assetFileNameToFingerprint = Path.GetFileName(newAssetRelativePath);
-            string fingerprint = asset.GetMetadata("Fingerprint");
-            string newAssetFingerprintedFileName = assetFileNameToFingerprint.Replace("#[.{fingerprint}]!", $".{fingerprint}");
-            if (newAssetFingerprintedFileName != assetFileNameToFingerprint)
-            {
-                newAssetItemSpec = $"{assetDirectory}/{newAssetFingerprintedFileName}";
-            }
-        }
-
-        var newAsset = new TaskItem(newAssetItemSpec, asset.CloneCustomMetadata());
-        newAsset.SetMetadata("RelativePath", newAssetRelativePath);
+        // Keep ItemSpec pointing to the actual file on disk.
+        // DefineStaticWebAssets will resolve fingerprint placeholders in RelativePath
+        // and compute Fingerprint/Integrity from the real file.
+        var newAsset = new TaskItem(asset.ItemSpec, asset.CloneCustomMetadata());
+        newAsset.SetMetadata("RelativePath", asset.GetMetadata("RelativePath"));
 
         ApplyPublishProperties(newAsset);
         return newAsset;
@@ -446,6 +434,10 @@ private void ComputeUpdatedAssemblies(
         // when the original assembly they depend on has been linked out.
         var assetsToUpdate = new Dictionary<string, ITaskItem>();
         var linkedAssets = new Dictionary<string, ITaskItem>();
+        // Secondary lookup by normalized filename for satellite matching.
+        // RelatedAsset may use a different base path (e.g., OutputPath/wwwroot)
+        // than the asset's build-time Identity (e.g., IntermediateOutputPath/webcil).
+        var assetsToUpdateByFileName = new Dictionary<string, string>(StringComparer.OrdinalIgnoreCase);
 
         foreach (var kvp in assemblyAssets)
         {
@@ -459,6 +451,8 @@ private void ComputeUpdatedAssemblies(
             {
                 // We found the assembly, so it'll have to be updated.
                 assetsToUpdate.Add(assetToUpdateItemSpec, asset);
+                if (!assetsToUpdateByFileName.ContainsKey(fileName))
+                    assetsToUpdateByFileName[fileName] = assetToUpdateItemSpec;
                 filesToRemove.Add(existing);
                 if (!string.Equals(asset.ItemSpec, existing.GetMetadata("FullPath"), StringComparison.Ordinal))
                 {
@@ -477,6 +471,18 @@ private void ComputeUpdatedAssemblies(
             var satelliteAssembly = kvp.Value;
             var relatedAsset = satelliteAssembly.GetMetadata("RelatedAsset");
 
+            // Try exact match first, then fall back to filename-based lookup.
+            // Normalize to .dll when webcil is enabled since assetsToUpdateByFileName
+            // keys are normalized to .dll (line 448) but RelatedAsset paths use .wasm.
+            var relatedAssetFileName = Path.GetFileName(relatedAsset);
+            if (IsWebCilEnabled)
+                relatedAssetFileName = Path.ChangeExtension(relatedAssetFileName, ".dll");
+            if (!assetsToUpdate.ContainsKey(relatedAsset)
+                && assetsToUpdateByFileName.TryGetValue(relatedAssetFileName, out var matchedKey))
+            {
+                relatedAsset = matchedKey;
+            }
+
             if (assetsToUpdate.ContainsKey(relatedAsset))
             {
                 assetsToUpdate.Add(satelliteAssembly.ItemSpec, satelliteAssembly);
@@ -590,9 +596,24 @@ private List<ITaskItem> ProcessCompressedAssets(
 
     private static void UpdateRelatedAssetProperty(ITaskItem asset, TaskItem newAsset, Dictionary<string, ITaskItem> updatedAssetsMap)
     {
-        if (!updatedAssetsMap.TryGetValue(asset.GetMetadata("RelatedAsset"), out var updatedRelatedAsset))
+        var relatedAsset = asset.GetMetadata("RelatedAsset");
+        if (!updatedAssetsMap.TryGetValue(relatedAsset, out var updatedRelatedAsset))
         {
-            throw new InvalidOperationException("Related asset not found.");
+            // Fall back to filename matching when RelatedAsset uses a different base path
+            // than the asset's build-time Identity (e.g., OutputPath/wwwroot vs obj/webcil).
+            var relatedBaseName = Path.GetFileNameWithoutExtension(relatedAsset);
+            foreach (var kvp in updatedAssetsMap)
+            {
+                if (string.Equals(Path.GetFileNameWithoutExtension(kvp.Key), relatedBaseName, StringComparison.OrdinalIgnoreCase))
+                {
+                    updatedRelatedAsset = kvp.Value;
+                    break;
+                }
+            }
+            if (updatedRelatedAsset == null)
+            {
+                throw new InvalidOperationException("Related asset not found.");
+            }
         }
 
         newAsset.SetMetadata("RelatedAsset", updatedRelatedAsset.ItemSpec);