diff --git a/src/Components/WebAssembly/Server/src/WebAssemblyRazorComponentsBuilderExtensions.cs b/src/Components/WebAssembly/Server/src/WebAssemblyRazorComponentsBuilderExtensions.cs
index 0dfb50ef840a..a55065ca9b45 100644
--- a/src/Components/WebAssembly/Server/src/WebAssemblyRazorComponentsBuilderExtensions.cs
+++ b/src/Components/WebAssembly/Server/src/WebAssemblyRazorComponentsBuilderExtensions.cs
@@ -1,6 +1,8 @@
 // Licensed to the .NET Foundation under one or more agreements.
 // The .NET Foundation licenses this file to you under the MIT license.
 
+using System.Diagnostics.CodeAnalysis;
+using System.Reflection;
 using Microsoft.AspNetCore.Components;
 using Microsoft.AspNetCore.Components.Authorization;
 using Microsoft.AspNetCore.Components.Endpoints.Infrastructure;
@@ -14,6 +16,9 @@ namespace Microsoft.Extensions.DependencyInjection;
 /// </summary>
 public static class WebAssemblyRazorComponentsBuilderExtensions
 {
+    private const string LazyAssemblyLoaderAssemblyName = "Microsoft.AspNetCore.Components.WebAssembly";
+    private const string LazyAssemblyLoaderTypeName = "Microsoft.AspNetCore.Components.WebAssembly.Services.LazyAssemblyLoader";
+
     /// <summary>
     /// Adds services to support rendering interactive WebAssembly components.
     /// </summary>
@@ -25,6 +30,15 @@ public static IRazorComponentsBuilder AddInteractiveWebAssemblyComponents(this I
 
         builder.Services.TryAddEnumerable(ServiceDescriptor.Singleton<RenderModeEndpointProvider, WebAssemblyEndpointProvider>());
 
+        // Try register LazyAssemblyLoader to prevent crashes during prerendering.
+        // TODO: Remove this once LazyAssemblyLoader is no longer used.
+        var lazyAssemblyLoaderType = GetLazyAssemblyLoaderType();
+
+        if (lazyAssemblyLoaderType != null)
+        {
+            builder.Services.TryAddScoped(lazyAssemblyLoaderType);
+        }
+
         return builder;
     }
 
@@ -46,4 +60,18 @@ public static IRazorComponentsBuilder AddAuthenticationStateSerialization(this I
 
         return builder;
     }
+
+    [DynamicDependency(DynamicallyAccessedMemberTypes.PublicConstructors, LazyAssemblyLoaderTypeName, LazyAssemblyLoaderAssemblyName)]
+    private static Type? GetLazyAssemblyLoaderType()
+    {
+        try
+        {
+            var assembly = Assembly.Load(LazyAssemblyLoaderAssemblyName);
+            return assembly.GetType(LazyAssemblyLoaderTypeName, throwOnError: false);
+        }
+        catch
+        {
+            return null;
+        }
+    }
 }
diff --git a/src/ProjectTemplates/test/Templates.Blazor.Tests/BlazorWebTemplateTest.cs b/src/ProjectTemplates/test/Templates.Blazor.Tests/BlazorWebTemplateTest.cs
index dc2cf5b63982..7a63733db354 100644
--- a/src/ProjectTemplates/test/Templates.Blazor.Tests/BlazorWebTemplateTest.cs
+++ b/src/ProjectTemplates/test/Templates.Blazor.Tests/BlazorWebTemplateTest.cs
@@ -1,6 +1,7 @@
 // Licensed to the .NET Foundation under one or more agreements.
 // The .NET Foundation licenses this file to you under the MIT license.
 
+using System.IO;
 using System.Net;
 using System.Net.Http;
 using System.Net.Http.Headers;
@@ -26,6 +27,18 @@ public async Task BlazorWebTemplate_Works(BrowserKind browserKind, string intera
             args: ["-int", interactivityOption],
             getTargetProject: GetTargetProject);
 
+        if (HasClientProject())
+        {
+            // In order to prevent an exception casued by missing LazyAssemblyLoader during pre-rendering,
+            // we are registering it into DI in AddInteractiveWebAssemblyComponents.
+            // To avoid adding new references between assemblies we try to resolve the type during run-time using reflection.
+            // This assert is here to check that the assembly containing LazyAssemblyLoader is actually present in a standard app
+            // created from the Blazor Web template.
+            // See https://github.com/dotnet/aspnetcore/issues/51966.
+            // TODO: Remove this when LazyAssemblyLoader is no longer being used, or the dependency graph changes so reflection is no longer needed.
+            AssertServerProjectCanUseLazyAssemblyLoader(GetTargetProject(project));
+        }
+
         // There won't be a counter page when the 'None' interactivity option is used
         var pagesToExclude = interactivityOption is "None"
             ? BlazorTemplatePages.Counter
@@ -92,4 +105,12 @@ private static async Task AssertWebAssemblyCompressionFormatAsync(AspNetProcess
         });
         Assert.Equal(expectedEncoding, response.Content.Headers.ContentEncoding.Single());
     }
+
+    private static void AssertServerProjectCanUseLazyAssemblyLoader(Project project)
+    {
+        var assemblyName = "Microsoft.AspNetCore.Components.WebAssembly.dll";
+        var fullPath = Path.Combine(project.TemplateBuildDir, assemblyName);
+        var doesExist = File.Exists(fullPath);
+        Assert.True(doesExist, "Required assembly does not exist");
+    }
 }