diff --git a/.autover/changes/fix-static-assets-non-production-env.json b/.autover/changes/fix-static-assets-non-production-env.json
new file mode 100644
index 000000000..60de53a47
--- /dev/null
+++ b/.autover/changes/fix-static-assets-non-production-env.json
@@ -0,0 +1,11 @@
+{
+  "Projects": [
+    {
+      "Name": "Amazon.Lambda.TestTool",
+      "Type": "Patch",
+      "ChangelogMessages": [
+        "Fixed static assets (CSS, JS, BlazorMonaco) failing to load when ASPNETCORE_ENVIRONMENT or DOTNET_ENVIRONMENT is set to a non-Production value by always serving static files from the tool's install directory."
+      ]
+    }
+  ]
+}
diff --git a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Amazon.Lambda.TestTool.csproj b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Amazon.Lambda.TestTool.csproj
index 9711bce5d..af6077d95 100644
--- a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Amazon.Lambda.TestTool.csproj
+++ b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Amazon.Lambda.TestTool.csproj
@@ -75,4 +75,13 @@
   <ItemGroup>
     <None Include="../../README.md" Pack="true" PackagePath="\" />
   </ItemGroup>
+
+
+  <!-- Ensure wwwroot content is copied to output directory -->
+  <ItemGroup>
+    <Content Update="wwwroot\**\*">
+      <CopyToOutputDirectory>PreserveNewest</CopyToOutputDirectory>
+    </Content>
+  </ItemGroup>
+
 </Project>
diff --git a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/TestToolProcess.cs b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/TestToolProcess.cs
index 61a0a8aa5..5da9d349b 100644
--- a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/TestToolProcess.cs
+++ b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/TestToolProcess.cs
@@ -60,10 +60,8 @@ public static TestToolProcess Startup(RunCommandSettings settings, CancellationT
         builder.Services.AddHttpContextAccessor();
 
         var wwwrootPath = Path.Combine(AppContext.BaseDirectory, "wwwroot");
-        if (builder.Environment.IsProduction())
-        {
-            builder.Services.AddSingleton<IFileProvider>(new PhysicalFileProvider(wwwrootPath));
-        }
+        var wwwrootFileProvider = new PhysicalFileProvider(wwwrootPath);
+        builder.Services.AddSingleton<IFileProvider>(wwwrootFileProvider);
         builder.Services.AddSingleton<IDirectoryManager, DirectoryManager>();
 
         var serviceHttp = $"http://{settings.LambdaEmulatorHost}:{settings.LambdaEmulatorPort}";
@@ -87,20 +85,21 @@ public static TestToolProcess Startup(RunCommandSettings settings, CancellationT
 
         var app = builder.Build();
 
-        if (app.Environment.IsProduction())
-        {
-            app.UseStaticFiles(new StaticFileOptions
-            {
-                FileProvider = new PhysicalFileProvider(wwwrootPath)
-            });
-        }
-        else
+        if (!app.Environment.IsProduction())
         {
             // nosemgrep: csharp.lang.security.stacktrace-disclosure.stacktrace-disclosure
             app.UseDeveloperExceptionPage();
-            app.UseStaticFiles();
         }
 
+        // Always use the explicit file provider to serve static files from the tool's install
+        // directory. Without this, non-Production environments attempt to use the static web
+        // assets manifest which contains absolute paths from the build machine and will fail
+        // when running as an installed global tool on a different machine.
+        app.UseStaticFiles(new StaticFileOptions
+        {
+            FileProvider = wwwrootFileProvider
+        });
+
         app.UseAntiforgery();
 
         app.MapRazorComponents<App>()