diff --git a/src/Components/Components/src/Rendering/Renderer.cs b/src/Components/Components/src/Rendering/Renderer.cs
index bf64cdf4a3..44904eb398 100644
--- a/src/Components/Components/src/Rendering/Renderer.cs
+++ b/src/Components/Components/src/Rendering/Renderer.cs
@@ -328,13 +328,14 @@ namespace Microsoft.AspNetCore.Components.Rendering
                     HandleException(task.Exception.GetBaseException());
                     break;
                 default:
-                    // We are not in rendering the root component.
-                    if (_pendingTasks == null)
-                    {
-                        return;
-                    }
+                    // It's important to evaluate the following even if we're not going to use
+                    // handledErrorTask below, because it has the side-effect of calling HandleException.
+                    var handledErrorTask = GetErrorHandledTask(task);
 
-                    _pendingTasks.Add(GetErrorHandledTask(task));
+                    // The pendingTasks collection is only used during prerendering to track quiescence,
+                    // so will be null at other times.
+                    _pendingTasks?.Add(handledErrorTask);
+                    
                     break;
             }
         }
diff --git a/src/Components/Components/test/RendererTest.cs b/src/Components/Components/test/RendererTest.cs
index 8d67ab50c9..df713ec9d5 100644
--- a/src/Components/Components/test/RendererTest.cs
+++ b/src/Components/Components/test/RendererTest.cs
@@ -2683,7 +2683,7 @@ namespace Microsoft.AspNetCore.Components.Test
         }
 
         [Fact]
-        public async Task ExceptionsThrownAsynchronouslyCanBeHandled()
+        public async Task ExceptionsThrownAsynchronouslyDuringFirstRenderCanBeHandled()
         {
             // Arrange
             var renderer = new TestRenderer { ShouldHandleExceptions = true };
@@ -2722,6 +2722,36 @@ namespace Microsoft.AspNetCore.Components.Test
             Assert.Same(exception, Assert.Single(renderer.HandledExceptions).GetBaseException());
         }
 
+        [Fact]
+        public async Task ExceptionsThrownAsynchronouslyAfterFirstRenderCanBeHandled()
+        {
+            // This differs from the "during first render" case, because some aspects of the rendering
+            // code paths are special cased for the first render because of prerendering.
+
+            // Arrange
+            var renderer = new TestRenderer { ShouldHandleExceptions = true };
+            var taskToAwait = Task.CompletedTask;
+            var component = new TestComponent(builder =>
+            {
+                builder.OpenComponent<ComponentThatAwaitsTask>(0);
+                builder.AddAttribute(1, nameof(ComponentThatAwaitsTask.TaskToAwait), taskToAwait);
+                builder.CloseComponent();
+            });
+            var componentId = renderer.AssignRootComponentId(component);
+            await renderer.RenderRootComponentAsync(componentId); // Not throwing on first render
+
+            var asyncExceptionTcs = new TaskCompletionSource<object>();
+            taskToAwait = asyncExceptionTcs.Task;
+            await renderer.Invoke(component.TriggerRender);
+
+            // Act
+            var exception = new InvalidOperationException();
+            asyncExceptionTcs.SetException(exception);
+
+            // Assert
+            Assert.Same(exception, Assert.Single(renderer.HandledExceptions).GetBaseException());
+        }
+
         [Fact]
         public async Task ExceptionsThrownAsynchronouslyFromMultipleComponentsCanBeHandled()
         {
@@ -3696,5 +3726,15 @@ namespace Microsoft.AspNetCore.Components.Test
                 OnAfterRenderAsync,
             }
         }
+
+        private class ComponentThatAwaitsTask : ComponentBase
+        {
+            [Parameter] public Task TaskToAwait { get; set; }
+
+            protected override async Task OnParametersSetAsync()
+            {
+                await TaskToAwait;
+            }
+        }
     }
 }