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 30970d18aa4eb9..e27f90693ea004 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
@@ -62,6 +62,7 @@ Copyright (c) .NET Foundation. All rights reserved.
 
     <!-- Compression -->
     <CompressionIncludePatterns>$(CompressionIncludePatterns);_framework\**</CompressionIncludePatterns>
+    <CompressionIncludePatterns Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true'"></CompressionIncludePatterns>
     <DisableBuildCompression Condition="'$(WasmBuildingForNestedPublish)' == 'true'">true</DisableBuildCompression>
   </PropertyGroup>
 
@@ -85,6 +86,8 @@ Copyright (c) .NET Foundation. All rights reserved.
     <EnableDefaultWasmAssembliesToBundle>false</EnableDefaultWasmAssembliesToBundle>
     <WasmNestedPublishAppDependsOn>_GatherWasmFilesToPublish;$(WasmNestedPublishAppDependsOn)</WasmNestedPublishAppDependsOn>
     <_WasmNestedPublishAppPreTarget>ComputeFilesToPublish</_WasmNestedPublishAppPreTarget>
+
+    <_WasmEnableHotReload Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true'">false</_WasmEnableHotReload>
   </PropertyGroup>
 
   <ItemGroup>
@@ -210,10 +213,12 @@ Copyright (c) .NET Foundation. All rights reserved.
       <_WasmInlineBootConfig Condition="'$(_WasmInlineBootConfig)' == ''">false</_WasmInlineBootConfig>
       <!-- true = wasm assets will have hard fingerprint; false = wasm assets won't have even soft fingerprint -->
       <_WasmFingerprintAssets>$(WasmFingerprintAssets)</_WasmFingerprintAssets>
+      <_WasmFingerprintAssets Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true'">false</_WasmFingerprintAssets>
       <_WasmFingerprintAssets Condition="'$(_WasmFingerprintAssets)' == '' and '$(_TargetingNET90OrLater)' == 'true'">true</_WasmFingerprintAssets>
       <_WasmFingerprintAssets Condition="'$(_WasmFingerprintAssets)' == ''">false</_WasmFingerprintAssets>
       <!-- true = dotnet.js will have hard fingerprint; false = dotnet.js will have soft fingerprint -->
       <_WasmFingerprintDotnetJs>$(WasmFingerprintDotnetJs)</_WasmFingerprintDotnetJs>
+      <_WasmFingerprintDotnetJs Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true'">false</_WasmFingerprintDotnetJs>
       <_WasmFingerprintDotnetJs Condition="'$(_WasmFingerprintDotnetJs)' == ''">$(OverrideHtmlAssetPlaceholders)</_WasmFingerprintDotnetJs>
       <_WasmFingerprintDotnetJs Condition="'$(_WasmFingerprintDotnetJs)' == ''">false</_WasmFingerprintDotnetJs>
       <_WasmBootConfigFileName>$(WasmBootConfigFileName)</_WasmBootConfigFileName>
@@ -661,6 +666,43 @@ Copyright (c) .NET Foundation. All rights reserved.
     </PropertyGroup>
   </Target>
 
+  <Target Name="EnsureProjectAssetsInOutputDirectoryForBundlerFriendlyBuild"
+          BeforeTargets="ResolveBuildStaticWebAssets"
+          Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true' and '$(IsPublishing)' != 'true'">
+    <!-- Fix non-publishing scenarios by copying project assets the way they are copied during publish,
+         so bundler-friendly builds are complete for the js bundler -->
+    <ItemGroup>
+      <StaticWebAsset Update="@(StaticWebAsset)" Condition="'%(StaticWebAsset.CopyToPublishDirectory)' != 'Never' and '%(StaticWebAsset.CopyToPublishDirectory)' != ''">
+        <CopyToOutputDirectory>%(StaticWebAsset.CopyToPublishDirectory)</CopyToOutputDirectory>
+      </StaticWebAsset>
+    </ItemGroup>
+  </Target>
+  
+  <Target Name="EnsurePublishAssetsInOutputDirectoryForBundlerFriendlyBuild"
+          AfterTargets="_SplitStaticWebAssetsByCopyOptions"
+          BeforeTargets="_BuildCopyStaticWebAssetsPreserveNewest;_BuildCopyStaticWebAssetsAlways;_BuildCopyStaticWebAssetsIfDifferent"
+          Condition="'$(WasmBundlerFriendlyBootConfig)' == 'true' and '$(IsPublishing)' != 'true'">
+    <!-- Fix non-publishing scenarios by manually adding the publish static web assets to the build static web assets 
+         so bundler-friendly builds are complete for the js bundler -->
+    <ComputeStaticWebAssetsForCurrentProject
+      Assets="@(StaticWebAsset)"
+      ProjectMode="$(StaticWebAssetProjectMode)"
+      AssetKind="Publish"
+      Source="$(PackageId)">
+      <Output TaskParameter="StaticWebAssets" ItemName="_StaticWebAssetsToCopy" />
+    </ComputeStaticWebAssetsForCurrentProject>
+    
+    <ComputeStaticWebAssetsTargetPaths Assets="@(_StaticWebAssetsToCopy)" PathPrefix="$(OutputPath)\wwwroot\">
+      <Output TaskParameter="AssetsWithTargetPath" ItemName="_StaticWebAssetsToCopyTargetPath" />
+    </ComputeStaticWebAssetsTargetPaths>
+
+    <ItemGroup>
+      <_BuildStaticWebAssetsCopyAlways Include="@(_StaticWebAssetsToCopyTargetPath)" Condition="'%(CopyToOutputDirectory)' == 'Always'" />
+      <_BuildStaticWebAssetsPreserveNewest Include="@(_StaticWebAssetsToCopyTargetPath)" Condition="'%(CopyToOutputDirectory)' == 'PreserveNewest'" />
+      <_BuildStaticWebAssetsIfDifferent Include="@(_StaticWebAssetsToCopyTargetPath)" Condition="'%(CopyToOutputDirectory)' == 'IfDifferent'" />
+    </ItemGroup>
+  </Target>
+  
   <!-- Publish starts here -->
 
   <!-- Make sure that ResolveAssemblyReferences runs early enough to ensure satellite assemblies are populated in the ResolvedFilesToPublish -->
diff --git a/src/mono/wasm/Wasm.Build.Tests/BuildTestBase.cs b/src/mono/wasm/Wasm.Build.Tests/BuildTestBase.cs
index 4e993991471be5..49c69733e88a1a 100644
--- a/src/mono/wasm/Wasm.Build.Tests/BuildTestBase.cs
+++ b/src/mono/wasm/Wasm.Build.Tests/BuildTestBase.cs
@@ -66,6 +66,7 @@ public abstract class BuildTestBase : IClassFixture<SharedBuildPerTestClassFixtu
         public static bool IsMonoRuntime => s_buildEnv.IsMonoRuntime;
         public static bool IsCoreClrRuntime => s_buildEnv.IsCoreClrRuntime;
         public static bool UseWebcil => s_buildEnv.UseWebcil;
+        public static bool UseJavascriptBundler => EnvironmentVariables.UseJavascriptBundler;
         public static string GetNuGetConfigPath()
             => Path.Combine(BuildEnvironment.TestDataPath, "nuget.config");
 
diff --git a/src/mono/wasm/Wasm.Build.Tests/DebugLevelTests.cs b/src/mono/wasm/Wasm.Build.Tests/DebugLevelTests.cs
index 47d1bc3c0426bf..d07d2864bdc671 100644
--- a/src/mono/wasm/Wasm.Build.Tests/DebugLevelTests.cs
+++ b/src/mono/wasm/Wasm.Build.Tests/DebugLevelTests.cs
@@ -112,4 +112,17 @@ public async Task PublishWithDefaultLevelAndPdbs(Configuration configuration)
         RunResult result = await RunForPublishWithWebServer(options);
         AssertDebugLevel(result.TestOutput, -1);
     }
+
+    [ConditionalFact(typeof(BuildTestBase), nameof(UseJavascriptBundler)), TestCategory("bundler-friendly")]
+    public void BundlerFriendlyBuildProvidesValidOutputForNpmBuild()
+    {
+        Configuration config = Configuration.Debug;
+        ProjectInfo info = CopyTestAsset(config, aot: false, TestAsset.WasmBasicTestApp, "DebugLevelTests_BundlerFriendlyBootConfigHasNoHotReloadLibraryInitializer");
+        // Project exists and contains <WasmBundlerFriendlyBootConfig>true</WasmBundlerFriendlyBootConfig>.
+        BuildProject(info, config, noDefaultOptions: true, wasmFingerprintDotnetJs: false);
+        string bootConfigPath = GetBootConfigPath(GetBinFrameworkDir(config, forPublish: false));
+        string bootJSObject = ProjectProviderBase.GetBootJsonContent(bootConfigPath);
+        // The bundler-friendly boot config is emitted as a JavaScript object literal, not JSON, so it cannot be parsed as JSON. It can still be inspected to ensure it does not contain hot reload.
+        Assert.DoesNotContain("Microsoft.DotNet.HotReload.WebAssembly.Browser", bootJSObject);
+    }
 }
diff --git a/src/mono/wasm/Wasm.Build.Tests/LibraryInitializerTests.cs b/src/mono/wasm/Wasm.Build.Tests/LibraryInitializerTests.cs
index 2ef6e921a754a2..809f41e8fca6ed 100644
--- a/src/mono/wasm/Wasm.Build.Tests/LibraryInitializerTests.cs
+++ b/src/mono/wasm/Wasm.Build.Tests/LibraryInitializerTests.cs
@@ -9,7 +9,6 @@
 using System.Text;
 using System.Text.RegularExpressions;
 using System.Threading.Tasks;
-using Microsoft.Playwright;
 using Xunit.Abstractions;
 using Xunit;
 
diff --git a/src/mono/wasm/Wasm.Build.Tests/Templates/WasmTemplateTestsBase.cs b/src/mono/wasm/Wasm.Build.Tests/Templates/WasmTemplateTestsBase.cs
index ee91db28f23c87..45ba5220a5c87a 100644
--- a/src/mono/wasm/Wasm.Build.Tests/Templates/WasmTemplateTestsBase.cs
+++ b/src/mono/wasm/Wasm.Build.Tests/Templates/WasmTemplateTestsBase.cs
@@ -20,9 +20,9 @@ namespace Wasm.Build.Tests;
 
 public class WasmTemplateTestsBase : BuildTestBase
 {
-    private readonly WasmSdkBasedProjectProvider _provider;
     private readonly string _extraBuildArgsBuild = "-p:WasmEnableHotReload=false";
     private readonly string _extraBuildArgsPublish = "-p:CompressionEnabled=false -p:WasmEnableHotReload=false";
+    private readonly WasmSdkBasedProjectProvider _provider;
     protected readonly PublishOptions _defaultPublishOptions;
     protected readonly BuildOptions _defaultBuildOptions;
     protected const string DefaultRuntimeAssetsRelativePath = "./_framework/";
@@ -119,8 +119,6 @@ protected ProjectInfo CopyTestAsset(
             extraProperties +=
             """
                 <WasmBundlerFriendlyBootConfig>true</WasmBundlerFriendlyBootConfig>
-                <WasmFingerprintAssets>false</WasmFingerprintAssets>
-                <CompressionEnabled>false</CompressionEnabled>
             """;
         }
 
@@ -190,9 +188,10 @@ public virtual (string projectDir, string buildOutput) PublishProject(
     public virtual (string projectDir, string buildOutput) BuildProject(
         ProjectInfo info,
         Configuration configuration,
+        bool noDefaultOptions = false,
         bool? isNativeBuild = null,
         bool? wasmFingerprintDotnetJs = null) => // null for unset properties
-        BuildProjectCore(info, configuration, _defaultBuildOptions, isNativeBuild, wasmFingerprintDotnetJs);
+        BuildProjectCore(info, configuration, noDefaultOptions ? new BuildOptions() : _defaultBuildOptions, isNativeBuild, wasmFingerprintDotnetJs);
 
     public virtual (string projectDir, string buildOutput) BuildProject(
         ProjectInfo info,
@@ -242,9 +241,9 @@ public virtual (string projectDir, string buildOutput) BuildProject(
             return (_projectDir, res.Output);
         }
 
-        if (EnvironmentVariables.UseJavascriptBundler && buildOptions.IsPublish)
+        if (EnvironmentVariables.UseJavascriptBundler)
         {
-            string publicWwwrootDir = Path.GetFullPath(Path.Combine(GetBinFrameworkDir(configuration, forPublish: true), ".."));
+            string publicWwwrootDir = Path.GetFullPath(Path.Combine(GetBinFrameworkDir(configuration, forPublish: buildOptions.IsPublish), ".."));
             File.Copy(Path.Combine(BuildEnvironment.TestAssetsPath, "JavascriptBundlers", "package.json"), Path.Combine(publicWwwrootDir, "package.json"));
             File.Copy(Path.Combine(BuildEnvironment.TestAssetsPath, "JavascriptBundlers", "rollup.config.mjs"), Path.Combine(publicWwwrootDir, "rollup.config.mjs"));
 
@@ -485,6 +484,9 @@ void OnErrorMessage(string msg)
         }
     }
 
+    public string GetBootConfigPath(string binFrameworkDir, string? bootConfigFileName = null) =>
+        _provider.GetBootConfigPath(binFrameworkDir, bootConfigFileName);
+
     public string GetBinFrameworkDir(Configuration config, bool forPublish, string? framework = null, string? projectDir = null) =>
         _provider.GetBinFrameworkDir(config, forPublish, framework ?? DefaultTargetFramework, projectDir);
 
diff --git a/src/mono/wasm/testassets/JavascriptBundlers/rollup.config.mjs b/src/mono/wasm/testassets/JavascriptBundlers/rollup.config.mjs
index f9ba590ed0b4b2..de79658c228003 100644
--- a/src/mono/wasm/testassets/JavascriptBundlers/rollup.config.mjs
+++ b/src/mono/wasm/testassets/JavascriptBundlers/rollup.config.mjs
@@ -13,7 +13,7 @@ export default {
    plugins: [
       files({
         output: 'public',
-        extensions: /\.(wasm|dat)$/,
+        extensions: /\.(wasm|dat|pdb)$/,
         hash: true,
       }),
       files({
@@ -39,4 +39,4 @@ export default {
          'process.env.NODE_ENV': '"production"'
       }),
    ]
-}
\ No newline at end of file
+}