diff --git a/src/Components/Server/src/Circuits/CircuitHost.cs b/src/Components/Server/src/Circuits/CircuitHost.cs
index 84649d0f7a9e..7acea8c63fa3 100644
--- a/src/Components/Server/src/Circuits/CircuitHost.cs
+++ b/src/Components/Server/src/Circuits/CircuitHost.cs
@@ -22,7 +22,7 @@ internal partial class CircuitHost : IAsyncDisposable
     private readonly CircuitOptions _options;
     private readonly RemoteNavigationManager _navigationManager;
     private readonly ILogger _logger;
-    private readonly Func<Func<Task>, Task> _dispatchInboundActivity;
+    private Func<Func<Task>, Task> _dispatchInboundActivity;
     private CircuitHandler[] _circuitHandlers;
     private bool _initialized;
     private bool _isFirstUpdate = true;
@@ -734,11 +734,10 @@ internal Task UpdateRootComponents(
 
         return Renderer.Dispatcher.InvokeAsync(async () =>
         {
-            var webRootComponentManager = Renderer.GetOrCreateWebRootComponentManager();
             var shouldClearStore = false;
+            var shouldWaitForQuiescence = false;
             var operations = operationBatch.Operations;
             var batchId = operationBatch.BatchId;
-            Task[]? pendingTasks = null;
             try
             {
                 if (Descriptors.Count > 0)
@@ -751,6 +750,7 @@ internal Task UpdateRootComponents(
                 if (_isFirstUpdate)
                 {
                     _isFirstUpdate = false;
+                    shouldWaitForQuiescence = true;
                     if (store != null)
                     {
                         shouldClearStore = true;
@@ -762,6 +762,7 @@ internal Task UpdateRootComponents(
 
                     // Retrieve the circuit handlers at this point.
                     _circuitHandlers = [.. _scope.ServiceProvider.GetServices<CircuitHandler>().OrderBy(h => h.Order)];
+                    _dispatchInboundActivity = BuildInboundActivityDispatcher(_circuitHandlers, Circuit);
                     await OnCircuitOpenedAsync(cancellation);
                     await OnConnectionUpAsync(cancellation);
 
@@ -773,44 +774,9 @@ internal Task UpdateRootComponents(
                             throw new InvalidOperationException($"The first set of update operations must always be of type {nameof(RootComponentOperationType.Add)}");
                         }
                     }
-
-                    pendingTasks = new Task[operations.Length];
-                }
-
-                for (var i = 0; i < operations.Length; i++)
-                {
-                    var operation = operations[i];
-                    switch (operation.Type)
-                    {
-                        case RootComponentOperationType.Add:
-                            var task = webRootComponentManager.AddRootComponentAsync(
-                                operation.SsrComponentId,
-                                operation.Descriptor.ComponentType,
-                                operation.Marker.Value.Key,
-                                operation.Descriptor.Parameters);
-                            if (pendingTasks != null)
-                            {
-                                pendingTasks[i] = task;
-                            }
-                            break;
-                        case RootComponentOperationType.Update:
-                            // We don't need to await component updates as any unhandled exception will be reported and terminate the circuit.
-                            _ = webRootComponentManager.UpdateRootComponentAsync(
-                                operation.SsrComponentId,
-                                operation.Descriptor.ComponentType,
-                                operation.Marker.Value.Key,
-                                operation.Descriptor.Parameters);
-                            break;
-                        case RootComponentOperationType.Remove:
-                            webRootComponentManager.RemoveRootComponent(operation.SsrComponentId);
-                            break;
-                    }
                 }
 
-                if (pendingTasks != null)
-                {
-                    await Task.WhenAll(pendingTasks);
-                }
+                await PerformRootComponentOperations(operations, shouldWaitForQuiescence);
 
                 await Client.SendAsync("JS.EndUpdateRootComponents", batchId);
 
@@ -836,6 +802,58 @@ internal Task UpdateRootComponents(
         });
     }
 
+    private async ValueTask PerformRootComponentOperations(
+        RootComponentOperation[] operations,
+        bool shouldWaitForQuiescence)
+    {
+        var webRootComponentManager = Renderer.GetOrCreateWebRootComponentManager();
+        var pendingTasks = shouldWaitForQuiescence
+            ? new Task[operations.Length]
+            : null;
+
+        // The inbound activity pipeline needs to be awaited because it populates
+        // the pending tasks used to wait for quiescence.
+        await HandleInboundActivityAsync(() =>
+        {
+            for (var i = 0; i < operations.Length; i++)
+            {
+                var operation = operations[i];
+                switch (operation.Type)
+                {
+                    case RootComponentOperationType.Add:
+                        var task = webRootComponentManager.AddRootComponentAsync(
+                            operation.SsrComponentId,
+                            operation.Descriptor.ComponentType,
+                            operation.Marker.Value.Key,
+                            operation.Descriptor.Parameters);
+                        if (pendingTasks != null)
+                        {
+                            pendingTasks[i] = task;
+                        }
+                        break;
+                    case RootComponentOperationType.Update:
+                        // We don't need to await component updates as any unhandled exception will be reported and terminate the circuit.
+                        _ = webRootComponentManager.UpdateRootComponentAsync(
+                            operation.SsrComponentId,
+                            operation.Descriptor.ComponentType,
+                            operation.Marker.Value.Key,
+                            operation.Descriptor.Parameters);
+                        break;
+                    case RootComponentOperationType.Remove:
+                        webRootComponentManager.RemoveRootComponent(operation.SsrComponentId);
+                        break;
+                }
+            }
+
+            return Task.CompletedTask;
+        });
+
+        if (pendingTasks != null)
+        {
+            await Task.WhenAll(pendingTasks);
+        }
+    }
+
     private static partial class Log
     {
         // 100s used for lifecycle stuff
diff --git a/src/Components/test/E2ETest/ServerRenderingTests/InteractivityTest.cs b/src/Components/test/E2ETest/ServerRenderingTests/InteractivityTest.cs
index d16ae8cf226b..cf894004da30 100644
--- a/src/Components/test/E2ETest/ServerRenderingTests/InteractivityTest.cs
+++ b/src/Components/test/E2ETest/ServerRenderingTests/InteractivityTest.cs
@@ -1133,6 +1133,14 @@ public void NavigationManagerCanRefreshSSRPageWhenServerInteractivityEnabled()
         Browser.Equal("GET", () => Browser.Exists(By.Id("method")).Text);
     }
 
+    [Fact]
+    public void InteractiveServerRootComponent_CanAccessCircuitContext()
+    {
+        Navigate($"{ServerPathBase}/interactivity/circuit-context");
+
+        Browser.Equal("True", () => Browser.FindElement(By.Id("has-circuit-context")).Text);
+    }
+
     private void BlockWebAssemblyResourceLoad()
     {
         ((IJavaScriptExecutor)Browser).ExecuteScript("sessionStorage.setItem('block-load-boot-resource', 'true')");
diff --git a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
index dead36b67e18..be68ef2ffd7e 100644
--- a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
+++ b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
@@ -8,6 +8,7 @@
 using Components.TestServer.RazorComponents;
 using Components.TestServer.RazorComponents.Pages.Forms;
 using Components.TestServer.Services;
+using Microsoft.AspNetCore.Components.Server.Circuits;
 using Microsoft.AspNetCore.Mvc;
 
 namespace TestServer;
@@ -35,6 +36,10 @@ public void ConfigureServices(IServiceCollection services)
         services.AddHttpContextAccessor();
         services.AddSingleton<AsyncOperationService>();
         services.AddCascadingAuthenticationState();
+
+        var circuitContextAccessor = new TestCircuitContextAccessor();
+        services.AddSingleton<CircuitHandler>(circuitContextAccessor);
+        services.AddSingleton(circuitContextAccessor);
     }
 
     // This method gets called by the runtime. Use this method to configure the HTTP request pipeline.
diff --git a/src/Components/test/testassets/Components.TestServer/RazorComponents/Pages/Interactivity/CircuitContextPage.razor b/src/Components/test/testassets/Components.TestServer/RazorComponents/Pages/Interactivity/CircuitContextPage.razor
new file mode 100644
index 000000000000..801358ec69f1
--- /dev/null
+++ b/src/Components/test/testassets/Components.TestServer/RazorComponents/Pages/Interactivity/CircuitContextPage.razor
@@ -0,0 +1,25 @@
+@page "/interactivity/circuit-context"
+@rendermode RenderMode.InteractiveServer
+@inject TestCircuitContextAccessor CircuitContextAccessor
+
+<h1>Circuit context</h1>
+
+<p>
+    Has circuit context: <span id="has-circuit-context">@_hasCircuitContext</span>
+</p>
+
+@code {
+    private bool _hasCircuitContext;
+
+    protected override async Task OnAfterRenderAsync(bool firstRender)
+    {
+        if (firstRender)
+        {
+            await Task.Yield();
+
+            _hasCircuitContext = CircuitContextAccessor.HasCircuitContext;
+
+            StateHasChanged();
+        }
+    }
+}