diff --git a/src/Components/Server/src/Circuits/CircuitFactory.cs b/src/Components/Server/src/Circuits/CircuitFactory.cs
index 0c086f054c03..a9aefb9fbfc9 100644
--- a/src/Components/Server/src/Circuits/CircuitFactory.cs
+++ b/src/Components/Server/src/Circuits/CircuitFactory.cs
@@ -93,6 +93,7 @@ public async ValueTask<CircuitHost> CreateCircuitHostAsync(
             resourceCollection);
 
         circuitActivitySource.Init(new Infrastructure.Server.ComponentsActivityLinkStore(renderer));
+        renderer.GetOrCreateWebRootComponentManager();
 
         // In Blazor Server we have already restored the app state, so we can get the handlers from DI.
         // In Blazor Web the state is provided in the first call to UpdateRootComponents, so we need to
diff --git a/src/Components/test/E2ETest/Tests/StatePersistanceJSRootTest.cs b/src/Components/test/E2ETest/Tests/StatePersistanceJSRootTest.cs
new file mode 100644
index 000000000000..9c554fccab79
--- /dev/null
+++ b/src/Components/test/E2ETest/Tests/StatePersistanceJSRootTest.cs
@@ -0,0 +1,42 @@
+// Licensed to the .NET Foundation under one or more agreements.
+// The .NET Foundation licenses this file to you under the MIT license.
+
+using Components.TestServer.RazorComponents;
+using Microsoft.AspNetCore.Components.E2ETest.Infrastructure;
+using Microsoft.AspNetCore.Components.E2ETest.Infrastructure.ServerFixtures;
+using Microsoft.AspNetCore.Components.E2ETests.ServerRenderingTests;
+using Microsoft.AspNetCore.Components.Web;
+using Microsoft.AspNetCore.E2ETesting;
+using OpenQA.Selenium;
+using TestServer;
+using Xunit.Abstractions;
+
+namespace Microsoft.AspNetCore.Components.E2ETests.Tests;
+
+// These tests are for Blazor Web implementation
+// For Blazor Server and Webassembly, check SaveStateTest.cs
+public class StatePersistanceJSRootTest : ServerTestBase<BasicTestAppServerSiteFixture<RazorComponentEndpointsStartup<App>>>
+{
+    public StatePersistanceJSRootTest(
+        BrowserFixture browserFixture,
+        BasicTestAppServerSiteFixture<RazorComponentEndpointsStartup<App>> serverFixture,
+        ITestOutputHelper output)
+        : base(browserFixture, serverFixture, output)
+    {
+        serverFixture.AdditionalArguments.AddRange("--RegisterDynamicJSRootComponent", "true");
+    }
+
+    [Theory]
+    [InlineData("ServerNonPrerendered")]
+    [InlineData("WebAssemblyNonPrerendered")]
+    public void PersistentStateIsSupportedInDynamicJSRoots(string renderMode)
+    {
+        Navigate($"subdir/WasmMinimal/dynamic-js-root.html?renderMode={renderMode}");
+
+        Browser.Equal("Counter", () => Browser.Exists(By.TagName("h1")).Text);
+        Browser.Equal("Current count: 0", () => Browser.Exists(By.CssSelector("p[role='status']")).Text);
+
+        Browser.Click(By.CssSelector("button.btn-primary"));
+        Browser.Equal("Current count: 1", () => Browser.Exists(By.CssSelector("p[role='status']")).Text);
+    }
+}
diff --git a/src/Components/test/testassets/Components.TestServer/Program.cs b/src/Components/test/testassets/Components.TestServer/Program.cs
index 568f809454a7..58e39b5d11c8 100644
--- a/src/Components/test/testassets/Components.TestServer/Program.cs
+++ b/src/Components/test/testassets/Components.TestServer/Program.cs
@@ -23,7 +23,8 @@ public static async Task Main(string[] args)
             ["Server authentication"] = (BuildWebHost<ServerAuthenticationStartup>(CreateAdditionalArgs(args)), "/subdir"),
             ["CORS (WASM)"] = (BuildWebHost<CorsStartup>(CreateAdditionalArgs(args)), "/subdir"),
             ["Prerendering (Server-side)"] = (BuildWebHost<PrerenderedStartup>(CreateAdditionalArgs(args)), "/prerendered"),
-            ["Razor Component Endpoints"] = (BuildWebHost<RazorComponentEndpointsStartup<Components.TestServer.RazorComponents.App>>(CreateAdditionalArgs(args)), "/subdir"),
+            ["Razor Component Endpoints"] = (BuildWebHost<RazorComponentEndpointsStartup<App>>(CreateAdditionalArgs(args)), "/subdir"),
+            ["Razor Component Endpoints with JS Root Component"] = (BuildWebHost<RazorComponentEndpointsStartup<App>>(CreateAdditionalArgs([.. args, "--RegisterDynamicJSRootComponent", "true"])), "/subdir"),
             ["Deferred component content (Server-side)"] = (BuildWebHost<DeferredComponentContentStartup>(CreateAdditionalArgs(args)), "/deferred-component-content"),
             ["Locked navigation (Server-side)"] = (BuildWebHost<LockedNavigationStartup>(CreateAdditionalArgs(args)), "/locked-navigation"),
             ["Client-side with fallback"] = (BuildWebHost<StartupWithMapFallbackToClientSideBlazor>(CreateAdditionalArgs(args)), "/fallback"),
diff --git a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
index 861e0fbdf288..986d4c391fd0 100644
--- a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
+++ b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
@@ -7,6 +7,7 @@
 using System.Web;
 using Components.TestServer.RazorComponents;
 using Components.TestServer.RazorComponents.Pages.Forms;
+using Components.TestServer.RazorComponents.Pages.PersistentState;
 using Components.TestServer.Services;
 using Microsoft.AspNetCore.Components;
 using Microsoft.AspNetCore.Components.Server.Circuits;
@@ -50,6 +51,10 @@ public void ConfigureServices(IServiceCollection services)
                     options.DisconnectedCircuitMaxRetained = 0;
                     options.DetailedErrors = true;
                 }
+                if (Configuration.GetValue<bool>("RegisterDynamicJSRootComponent"))
+                {
+                    options.RootComponents.RegisterForJavaScript<TestContentPackage.PersistentComponents.ComponentWithPersistentState>("dynamic-js-root-counter");
+                }
             })
             .AddAuthenticationStateSerialization(options =>
             {
diff --git a/src/Components/test/testassets/Components.WasmMinimal/Pages/CounterWithPersistentState.razor b/src/Components/test/testassets/Components.WasmMinimal/Pages/CounterWithPersistentState.razor
new file mode 100644
index 000000000000..f44a4a80f1ac
--- /dev/null
+++ b/src/Components/test/testassets/Components.WasmMinimal/Pages/CounterWithPersistentState.razor
@@ -0,0 +1,23 @@
+@page "/persistent-state/counter"
+
+<TestContentPackage.PersistentComponents.ComponentWithPersistentState @rendermode="@RenderModeHelper.GetRenderMode(_renderMode)"/>
+
+
+@code{
+    [Parameter, SupplyParameterFromQuery(Name = "renderMode")]
+    public string? RenderModeStr { get; set; }
+
+    private RenderModeId _renderMode;
+
+    protected override void OnInitialized()
+    {
+        if (!string.IsNullOrEmpty(RenderModeStr))
+        {
+            _renderMode = RenderModeHelper.ParseRenderMode(RenderModeStr);
+        }
+        else
+        {
+            throw new ArgumentException("RenderModeStr cannot be null or empty", nameof(RenderModeStr));
+        }
+    }
+}
\ No newline at end of file
diff --git a/src/Components/test/testassets/Components.WasmMinimal/wwwroot/dynamic-js-root.html b/src/Components/test/testassets/Components.WasmMinimal/wwwroot/dynamic-js-root.html
new file mode 100644
index 000000000000..284a4d151a11
--- /dev/null
+++ b/src/Components/test/testassets/Components.WasmMinimal/wwwroot/dynamic-js-root.html
@@ -0,0 +1,16 @@
+<html>
+<head>
+  <base href="/subdir/" />
+</head>
+<body>
+  <div id="app">
+  </div>
+
+  <script src="_framework/blazor.server.js" autostart="false"></script>
+  <script>
+    Blazor.start().then(() => {
+      Blazor.rootComponents.add(document.getElementById("app"), "dynamic-js-root-counter", {});
+    });
+  </script>
+</body>
+</html>
diff --git a/src/Components/test/testassets/TestContentPackage/PersistentComponents/ComponentWithPersistentState.razor b/src/Components/test/testassets/TestContentPackage/PersistentComponents/ComponentWithPersistentState.razor
new file mode 100644
index 000000000000..d26ae13fc390
--- /dev/null
+++ b/src/Components/test/testassets/TestContentPackage/PersistentComponents/ComponentWithPersistentState.razor
@@ -0,0 +1,16 @@
+<PageTitle>Counter</PageTitle>
+
+<h1>Counter</h1>
+
+<p role="status">Current count: @currentCount</p>
+
+<button class="btn btn-primary" @onclick="IncrementCount">Click me</button>
+
+@code {
+    [PersistentState] public int currentCount { get; set; }
+
+    private void IncrementCount()
+    {
+        currentCount++;
+    }
+}