diff --git a/src/mono/wasm/Wasm.Build.Tests/SatelliteLoadingTests.cs b/src/mono/wasm/Wasm.Build.Tests/SatelliteLoadingTests.cs
index 90d27ad7287c76..c0bc8895e093fb 100644
--- a/src/mono/wasm/Wasm.Build.Tests/SatelliteLoadingTests.cs
+++ b/src/mono/wasm/Wasm.Build.Tests/SatelliteLoadingTests.cs
@@ -47,10 +47,12 @@ public async Task LoadSatelliteAssembly(bool loadAllSatelliteResources)
             // So there messages are should be present only when we are lazily loading satellites.
             expectedOutput.Add(m => Assert.Equal("default: hello", m));
             expectedOutput.Add(m => Assert.Equal("es-ES without satellite: hello", m));
+            expectedOutput.Add(m => Assert.Equal("fr-FR without satellite: hello", m));
         }
 
         expectedOutput.Add(m => Assert.Equal("default: hello", m));
         expectedOutput.Add(m => Assert.Equal("es-ES with satellite: hola", m));
+        expectedOutput.Add(m => Assert.Equal("fr-FR with satellite: bonjour", m));
 
         Assert.Collection(
             result.TestOutput,
@@ -68,7 +70,7 @@ public async Task LoadSatelliteAssemblyFromReference()
         var appCsprojPath = Path.Combine(_projectDir, "WasmBasicTestApp.csproj");
         var appCsproj = XDocument.Load(appCsprojPath);
 
-        var projectReference = appCsproj.Descendants("ProjectReference").Where(pr => pr.Attribute("Include")?.Value?.Contains("ResourceLibrary") ?? false).Single();
+        var projectReference = appCsproj.Descendants("ProjectReference").Single(pr => pr.Attribute("Include")?.Value?.Contains("ResourceLibrary") ?? false);
         var itemGroup = projectReference.Parent!;
         projectReference.Remove();
 
@@ -94,8 +96,32 @@ public async Task LoadSatelliteAssemblyFromReference()
             result.TestOutput,
             m => Assert.Equal("default: hello", m),
             m => Assert.Equal("es-ES without satellite: hello", m),
+            m => Assert.Equal("fr-FR without satellite: hello", m),
             m => Assert.Equal("default: hello", m),
-            m => Assert.Equal("es-ES with satellite: hola", m)
+            m => Assert.Equal("es-ES with satellite: hola", m),
+            m => Assert.Equal("fr-FR with satellite: bonjour", m)
         );
     }
+
+    [Fact, TestCategory("no-fingerprinting")]
+    public void SatelliteAssembliesFromPackageReference()
+    {
+        Configuration config = Configuration.Release;
+        ProjectInfo info = CopyTestAsset(config, false, TestAsset.WasmBasicTestApp, "SatelliteLoadingTestsFromPackageReference");
+        BuildProject(info, config, new BuildOptions(ExtraMSBuildArgs: "-p:TestSatelliteAssembliesFromPackage=true"));
+
+        string binFrameworkDir = GetBinFrameworkDir(config, forPublish: false);
+
+        // Microsoft.CodeAnalysis.CSharp has satellite assemblies for multiple locales
+        // Verify that at least some of them are present in the AppBundle
+        string[] expectedLocales = ["cs", "de", "es", "fr", "it", "ja", "ko", "pl", "pt-BR", "ru", "tr", "zh-Hans", "zh-Hant"];
+        foreach (string locale in expectedLocales)
+        {
+            string satelliteDir = Path.Combine(binFrameworkDir, locale);
+            Assert.True(Directory.Exists(satelliteDir), $"Expected satellite directory '{locale}' to exist in {binFrameworkDir}");
+
+            string[] satelliteFiles = Directory.GetFiles(satelliteDir, "Microsoft.CodeAnalysis.CSharp.resources*");
+            Assert.True(satelliteFiles.Length > 0, $"Expected Microsoft.CodeAnalysis.CSharp.resources.dll in {satelliteDir}");
+        }
+    }
 }
diff --git a/src/mono/wasm/testassets/WasmBasicTestApp/App/SatelliteAssembliesTest.cs b/src/mono/wasm/testassets/WasmBasicTestApp/App/SatelliteAssembliesTest.cs
index 8d7631e0c8f6ce..92a695d284e0cd 100644
--- a/src/mono/wasm/testassets/WasmBasicTestApp/App/SatelliteAssembliesTest.cs
+++ b/src/mono/wasm/testassets/WasmBasicTestApp/App/SatelliteAssembliesTest.cs
@@ -13,7 +13,7 @@ public static async Task Run(bool loadSatelliteAssemblies)
         if (loadSatelliteAssemblies)
         {
             ResourceLibrary.ResourceAccessor.Read(TestOutput.WriteLine, false);
-            await LoadSatelliteAssemblies(new[] { "es-ES" });
+            await LoadSatelliteAssemblies(new[] { "es-ES", "fr-FR" });
         }
 
         ResourceLibrary.ResourceAccessor.Read(TestOutput.WriteLine, true);
diff --git a/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceAccessor.cs b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceAccessor.cs
index 27073846c66ae7..7c48551cabb3d8 100644
--- a/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceAccessor.cs
+++ b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceAccessor.cs
@@ -15,5 +15,6 @@ public static void Read(Action<string> testOuput, bool hasSatellites)
         var rm = new ResourceManager("ResourceLibrary.words", typeof(ResourceAccessor).Assembly);
         testOuput($"default: {rm.GetString("hello", CultureInfo.CurrentCulture)}");
         testOuput($"es-ES {(hasSatellites ? "with" : "without")} satellite: {rm.GetString("hello", new CultureInfo("es-ES"))}");
+        testOuput($"fr-FR {(hasSatellites ? "with" : "without")} satellite: {rm.GetString("hello", new CultureInfo("fr-FR"))}");
     }
 }
diff --git a/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceLibrary.csproj b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceLibrary.csproj
index 9a4419fdc08de5..8511ea8189bd03 100644
--- a/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceLibrary.csproj
+++ b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/ResourceLibrary.csproj
@@ -4,4 +4,8 @@
     <OutputType>Library</OutputType>
     <AllowUnsafeBlocks>true</AllowUnsafeBlocks>
   </PropertyGroup>
+
+  <ItemGroup Condition="'$(TestSatelliteAssembliesFromPackage)' == 'true'">
+    <PackageReference Include="Microsoft.CodeAnalysis.CSharp" Version="5.0.0" />
+  </ItemGroup>
 </Project>
diff --git a/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/words.fr-FR.resx b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/words.fr-FR.resx
new file mode 100644
index 00000000000000..61280687cdc2bd
--- /dev/null
+++ b/src/mono/wasm/testassets/WasmBasicTestApp/ResourceLibrary/words.fr-FR.resx
@@ -0,0 +1,127 @@
+<?xml version="1.0" encoding="utf-8"?>
+<root>
+  <!--
+    Microsoft ResX Schema
+
+    Version 2.0
+
+    The primary goals of this format is to allow a simple XML format
+    that is mostly human readable. The generation and parsing of the
+    various data types are done through the TypeConverter classes
+    associated with the data types.
+
+    Example:
+
+    ... ado.net/XML headers & schema ...
+    <resheader name="resmimetype">text/microsoft-resx</resheader>
+    <resheader name="version">2.0</resheader>
+    <resheader name="reader">System.Resources.ResXResourceReader, System.Windows.Forms, ...</resheader>
+    <resheader name="writer">System.Resources.ResXResourceWriter, System.Windows.Forms, ...</resheader>
+    <data name="Name1"><value>this is my long string</value><comment>this is a comment</comment></data>
+    <data name="Color1" type="System.Drawing.Color, System.Drawing">Blue</data>
+    <data name="Bitmap1" mimetype="application/x-microsoft.net.object.binary.base64">
+        <value>[base64 mime encoded serialized .NET Framework object]</value>
+    </data>
+    <data name="Icon1" type="System.Drawing.Icon, System.Drawing" mimetype="application/x-microsoft.net.object.bytearray.base64">
+        <value>[base64 mime encoded string representing a byte array form of the .NET Framework object]</value>
+        <comment>This is a comment</comment>
+    </data>
+
+    There are any number of "resheader" rows that contain simple
+    name/value pairs.
+
+    Each data row contains a name, and value. The row also contains a
+    type or mimetype. Type corresponds to a .NET class that support
+    text/value conversion through the TypeConverter architecture.
+    Classes that don't support this are serialized and stored with the
+    mimetype set.
+
+    The mimetype is used for serialized objects, and tells the
+    ResXResourceReader how to depersist the object. This is currently not
+    extensible. For a given mimetype the value must be set accordingly:
+
+    Note - application/x-microsoft.net.object.binary.base64 is the format
+    that the ResXResourceWriter will generate, however the reader can
+    read any of the formats listed below.
+
+    mimetype: application/x-microsoft.net.object.binary.base64
+    value   : The object must be serialized with
+            : System.Runtime.Serialization.Formatters.Binary.BinaryFormatter
+            : and then encoded with base64 encoding.
+
+    mimetype: application/x-microsoft.net.object.soap.base64
+    value   : The object must be serialized with
+            : System.Runtime.Serialization.Formatters.Soap.SoapFormatter
+            : and then encoded with base64 encoding.
+
+    mimetype: application/x-microsoft.net.object.bytearray.base64
+    value   : The object must be serialized into a byte array
+            : using a System.ComponentModel.TypeConverter
+            : and then encoded with base64 encoding.
+    -->
+  <xsd:schema id="root" xmlns="" xmlns:xsd="http://www.w3.org/2001/XMLSchema" xmlns:msdata="urn:schemas-microsoft-com:xml-msdata">
+    <xsd:import namespace="http://www.w3.org/XML/1998/namespace" />
+    <xsd:element name="root" msdata:IsDataSet="true">
+      <xsd:complexType>
+        <xsd:choice maxOccurs="unbounded">
+          <xsd:element name="metadata">
+            <xsd:complexType>
+              <xsd:sequence>
+                <xsd:element name="value" type="xsd:string" minOccurs="0" />
+              </xsd:sequence>
+              <xsd:attribute ref="xml:space" />
+              <xsd:attribute name="name" use="required" type="xsd:string" />
+              <xsd:attribute name="type" type="xsd:string" />
+              <xsd:attribute name="mimetype" type="xsd:string" />
+            </xsd:complexType>
+          </xsd:element>
+          <xsd:element name="assembly">
+            <xsd:complexType>
+              <xsd:attribute name="alias" type="xsd:string" />
+              <xsd:attribute name="name" type="xsd:string" />
+            </xsd:complexType>
+          </xsd:element>
+          <xsd:element name="data">
+            <xsd:complexType>
+              <xsd:sequence>
+                <xsd:element name="value" type="xsd:string" minOccurs="0" msdata:Ordinal="1" />
+                <xsd:element name="comment" type="xsd:string" minOccurs="0" msdata:Ordinal="2" />
+              </xsd:sequence>
+              <xsd:attribute name="name" type="xsd:string" use="required" msdata:Ordinal="1" />
+              <xsd:attribute name="type" type="xsd:string" msdata:Ordinal="3" />
+              <xsd:attribute name="mimetype" type="xsd:string" msdata:Ordinal="4" />
+              <xsd:attribute ref="xml:space" />
+            </xsd:complexType>
+          </xsd:element>
+          <xsd:element name="resheader">
+            <xsd:complexType>
+              <xsd:sequence>
+                <xsd:element name="value" type="xsd:string" minOccurs="0" msdata:Ordinal="1" />
+              </xsd:sequence>
+              <xsd:attribute name="name" type="xsd:string" use="required" />
+            </xsd:complexType>
+          </xsd:element>
+        </xsd:choice>
+      </xsd:complexType>
+    </xsd:element>
+  </xsd:schema>
+  <resheader name="resmimetype">
+    <value>text/microsoft-resx</value>
+  </resheader>
+  <resheader name="version">
+    <value>2.0</value>
+  </resheader>
+  <resheader name="reader">
+    <value>System.Resources.ResXResourceReader, System.Windows.Forms, Version=4.0.0.0, Culture=neutral, PublicKeyToken=b77a5c561934e089</value>
+  </resheader>
+  <resheader name="writer">
+    <value>System.Resources.ResXResourceWriter, System.Windows.Forms, Version=4.0.0.0, Culture=neutral, PublicKeyToken=b77a5c561934e089</value>
+  </resheader>
+  <data name="bye" xml:space="preserve">
+    <value>au revoir</value>
+  </data>
+  <assembly alias="System.Windows.Forms" name="System.Windows.Forms, Version=4.0.0.0, Culture=neutral, PublicKeyToken=b77a5c561934e089" />
+  <data name="hello" xml:space="preserve">
+    <value>bonjour</value>
+  </data>
+</root>
diff --git a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmBuildAssets.cs b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmBuildAssets.cs
index 2eafa784282373..34dcf1647aa3e2 100644
--- a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmBuildAssets.cs
+++ b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/ComputeWasmBuildAssets.cs
@@ -66,7 +66,7 @@ public override bool Execute()
     {
         var filesToRemove = new List<ITaskItem>();
         var assetCandidates = new List<ITaskItem>();
-        var uniqueFileNames = new HashSet<string>(StringComparer.OrdinalIgnoreCase);
+        var uniqueRelativePaths = new HashSet<string>(StringComparer.OrdinalIgnoreCase);
 
         try
         {
@@ -117,46 +117,49 @@ public override bool Execute()
 
                     assetCandidate.SetMetadata("RelatedAsset", Path.GetFullPath(Path.Combine(OutputPath, "wwwroot", "_framework", Path.GetFileName(resolvedFrom))));
 
-                    assetCandidates.Add(assetCandidate);
-                    continue;
+                    candidate = assetCandidate;
                 }
-
-                string relativePath = AssetsComputingHelper.GetCandidateRelativePath(candidate, FingerprintAssets, FingerprintDotNetJs);
-                candidate.SetMetadata("RelativePath", relativePath);
-
-                // Workaround for https://github.com/dotnet/aspnetcore/issues/37574.
-                // For items added as "Reference" in project references, the OriginalItemSpec is incorrect.
-                // Ignore it, and use the FullPath instead.
-                if (candidate.GetMetadata("ReferenceSourceTarget") == "ProjectReference")
+                else
                 {
-                    candidate.SetMetadata("OriginalItemSpec", candidate.ItemSpec);
+                    var culture = candidate.GetMetadata("Culture");
+                    if (!string.IsNullOrEmpty(culture))
+                    {
+                        candidate.SetMetadata("AssetKind", "Build");
+                        candidate.SetMetadata("AssetRole", "Related");
+                        candidate.SetMetadata("AssetTraitName", "Culture");
+                        candidate.SetMetadata("AssetTraitValue", culture);
+
+                        var fileName = candidate.GetMetadata("FileName");
+                        var suffixIndex = fileName.Length - ".resources".Length;
+                        var relatedAssetPath = Path.GetFullPath(Path.Combine(
+                            OutputPath,
+                            "wwwroot",
+                            "_framework",
+                            fileName.Substring(0, suffixIndex) + ProjectAssembly[0].GetMetadata("Extension")));
+
+                        candidate.SetMetadata("RelatedAsset", relatedAssetPath);
+                        candidate.SetMetadata("RelativePath", $"_framework/{culture}/{fileName}{candidate.GetMetadata("Extension")}");
+
+                        Log.LogMessage(MessageImportance.Low, "Found satellite assembly '{0}' asset for inferred candidate '{1}' with culture '{2}'", candidate.ItemSpec, relatedAssetPath, culture);
+                    }
+                    else
+                    {
+                        // Workaround for https://github.com/dotnet/aspnetcore/issues/37574.
+                        // For items added as "Reference" in project references, the OriginalItemSpec is incorrect.
+                        // Ignore it, and use the FullPath instead.
+                        if (candidate.GetMetadata("ReferenceSourceTarget") == "ProjectReference")
+                        {
+                            candidate.SetMetadata("OriginalItemSpec", candidate.ItemSpec);
+                        }
+
+                        candidate.SetMetadata("RelativePath", AssetsComputingHelper.GetCandidateRelativePath(candidate, FingerprintAssets, FingerprintDotNetJs));
+                    }
                 }
 
-                var culture = candidate.GetMetadata("Culture");
-                if (!string.IsNullOrEmpty(culture))
+                var relativePath = candidate.GetMetadata("RelativePath");
+                if (!uniqueRelativePaths.Add(relativePath))
                 {
-                    candidate.SetMetadata("AssetKind", "Build");
-                    candidate.SetMetadata("AssetRole", "Related");
-                    candidate.SetMetadata("AssetTraitName", "Culture");
-                    candidate.SetMetadata("AssetTraitValue", culture);
-                    var fileName = candidate.GetMetadata("FileName");
-                    var suffixIndex = fileName.Length - ".resources".Length;
-                    var relatedAssetPath = Path.GetFullPath(Path.Combine(
-                        OutputPath,
-                        "wwwroot",
-                        "_framework",
-                        fileName.Substring(0, suffixIndex) + ProjectAssembly[0].GetMetadata("Extension")));
-
-                    candidate.SetMetadata("RelatedAsset", relatedAssetPath);
-
-                    Log.LogMessage(MessageImportance.Low, "Found satellite assembly '{0}' asset for inferred candidate '{1}' with culture '{2}'", candidate.ItemSpec, relatedAssetPath, culture);
-                }
-
-                // Check for unique file name before adding candidate
-                var candidateFileName = Path.GetFileName(candidate.ItemSpec);
-                if (!uniqueFileNames.Add(candidateFileName))
-                {
-                    Log.LogMessage(MessageImportance.Low, "Skipping duplicate file name '{0}' for candidate '{1}'", candidateFileName, candidate.ItemSpec);
+                    Log.LogMessage(MessageImportance.Low, "Skipping duplicate relative path '{0}' for candidate '{1}'", relativePath, candidate.ItemSpec);
                     continue;
                 }
 
@@ -191,13 +194,18 @@ public override bool Execute()
                     "_framework",
                     ProjectAssembly[0].GetMetadata("FileName") + ProjectAssembly[0].GetMetadata("Extension")));
 
-                var normalizedPath = assetCandidate.GetMetadata("TargetPath").Replace('\\', '/');
+                var relativePath = $"_framework/{assetCandidate.GetMetadata("TargetPath").Replace('\\', '/')}";
+                if (!uniqueRelativePaths.Add(relativePath))
+                {
+                    Log.LogMessage(MessageImportance.Low, "Skipping duplicate relative path '{0}' for candidate '{1}'", relativePath, projectSatelliteAssembly.ItemSpec);
+                    continue;
+                }
 
                 assetCandidate.SetMetadata("AssetKind", "Build");
                 assetCandidate.SetMetadata("AssetRole", "Related");
                 assetCandidate.SetMetadata("AssetTraitName", "Culture");
                 assetCandidate.SetMetadata("AssetTraitValue", candidateCulture);
-                assetCandidate.SetMetadata("RelativePath", Path.Combine("_framework", normalizedPath));
+                assetCandidate.SetMetadata("RelativePath", relativePath);
                 assetCandidate.SetMetadata("RelatedAsset", projectAssemblyAssetPath);
 
                 assetCandidates.Add(assetCandidate);