diff --git a/src/Aspire.Hosting/Dcp/DcpExecutor.cs b/src/Aspire.Hosting/Dcp/DcpExecutor.cs
index 2b3bd106e20..da9ed8739c0 100644
--- a/src/Aspire.Hosting/Dcp/DcpExecutor.cs
+++ b/src/Aspire.Hosting/Dcp/DcpExecutor.cs
@@ -1581,6 +1581,7 @@ private static (string, EndpointBindingMode) NormalizeTargetHost(string targetHo
         {
             null or "" => ("localhost", EndpointBindingMode.SingleAddress), // Default is localhost
             var s when string.Equals(s, "localhost", StringComparison.OrdinalIgnoreCase) => ("localhost", EndpointBindingMode.SingleAddress), // Explicitly set to localhost
+            var s when s.Length > 10 && s.EndsWith(".localhost", StringComparison.OrdinalIgnoreCase) => ("localhost", EndpointBindingMode.SingleAddress), // Explicitly set to localhost when using .localhost subdomain
             var s when IPAddress.TryParse(s, out var ipAddress) => ipAddress switch // The host is an IP address
             {
                 var ip when IPAddress.Any.Equals(ip) => ("localhost", EndpointBindingMode.IPv4AnyAddresses), // 0.0.0.0 (IPv4 all addresses)
diff --git a/src/Aspire.Hosting/Orchestrator/ApplicationOrchestrator.cs b/src/Aspire.Hosting/Orchestrator/ApplicationOrchestrator.cs
index 153431f6b96..709cc47000b 100644
--- a/src/Aspire.Hosting/Orchestrator/ApplicationOrchestrator.cs
+++ b/src/Aspire.Hosting/Orchestrator/ApplicationOrchestrator.cs
@@ -212,8 +212,23 @@ private async Task ProcessResourceUrlCallbacks(IResource resource, CancellationT
                 Debug.Assert(endpoint.AllocatedEndpoint is not null, "Endpoint should be allocated at this point as we're calling this from ResourceEndpointsAllocatedEvent handler.");
                 if (endpoint.AllocatedEndpoint is { } allocatedEndpoint)
                 {
-                    var url = new ResourceUrlAnnotation { Url = allocatedEndpoint.UriString, Endpoint = new EndpointReference(resourceWithEndpoints, endpoint) };
+                    var endpointReference = new EndpointReference(resourceWithEndpoints, endpoint);
+                    var url = new ResourceUrlAnnotation { Url = allocatedEndpoint.UriString, Endpoint = endpointReference };
                     urls.Add(url);
+                    if (allocatedEndpoint.BindingMode != EndpointBindingMode.SingleAddress && (endpoint.TargetHost is not "localhost" or "127.0.0.1"))
+                    {
+                        // Endpoint is listening on multiple addresses so add another URL based on the declared target hostname
+                        // For endpoints targeting all external addresses (IPv4 0.0.0.0 or IPv6 ::) use the machine name
+                        var address = endpoint.TargetHost is "0.0.0.0" or "::" ? Environment.MachineName : endpoint.TargetHost;
+                        url = new ResourceUrlAnnotation { Url = $"{allocatedEndpoint.UriScheme}://{address}:{allocatedEndpoint.Port}", Endpoint = endpointReference };
+                        urls.Add(url);
+                    }
+                    else if (endpoint.TargetHost.Length > 10 && endpoint.TargetHost.EndsWith(".localhost", StringComparison.OrdinalIgnoreCase))
+                    {
+                        // Add the originally declared *.localhost URL
+                        url = new ResourceUrlAnnotation { Url = $"{allocatedEndpoint.UriScheme}://{endpoint.TargetHost}:{allocatedEndpoint.Port}", Endpoint = endpointReference };
+                        urls.Add(url);
+                    }
                 }
             }
         }
diff --git a/tests/Aspire.Hosting.Tests/WithEndpointTests.cs b/tests/Aspire.Hosting.Tests/WithEndpointTests.cs
index 32c25dc9fd1..1a2fbcbec4b 100644
--- a/tests/Aspire.Hosting.Tests/WithEndpointTests.cs
+++ b/tests/Aspire.Hosting.Tests/WithEndpointTests.cs
@@ -617,6 +617,72 @@ public void WithEndpoint_WithAllArguments_ForwardsAllArguments()
         Assert.Equal(System.Net.Sockets.ProtocolType.Tcp, endpoint.Protocol);
     }
 
+    [Fact]
+    public async Task LocalhostTopLevelDomainSetsAnnotationValues()
+    {
+        using var builder = TestDistributedApplicationBuilder.Create();
+
+        var tcs = new TaskCompletionSource();
+        var projectA = builder.AddProject<ProjectA>("projecta")
+            .WithHttpsEndpoint()
+            .WithEndpoint("https", e => e.TargetHost = "example.localhost", createIfNotExists: false)
+            .OnBeforeResourceStarted((_, _, _) =>
+            {
+                tcs.SetResult();
+                return Task.CompletedTask;
+            });
+
+        var app = await builder.BuildAsync();
+        await app.StartAsync();
+        await tcs.Task;
+
+        var urls = projectA.Resource.Annotations.OfType<ResourceUrlAnnotation>();
+        Assert.Collection(urls,
+            url => Assert.StartsWith("https://localhost:", url.Url),
+            url => Assert.StartsWith("https://example.localhost:", url.Url));
+
+        EndpointAnnotation endpoint = Assert.Single(projectA.Resource.Annotations.OfType<EndpointAnnotation>());
+        Assert.NotNull(endpoint.AllocatedEndpoint);
+        Assert.Equal(EndpointBindingMode.SingleAddress, endpoint.AllocatedEndpoint.BindingMode);
+        Assert.Equal("localhost", endpoint.AllocatedEndpoint.Address);
+
+        await app.StopAsync();
+    }
+
+    [Theory]
+    [InlineData("0.0.0.0", EndpointBindingMode.IPv4AnyAddresses)]
+    //[InlineData("::", EndpointBindingMode.IPv6AnyAddresses)] // Need to figure out a good way to check that Ipv6 binding is supported
+    public async Task TopLevelDomainSetsAnnotationValues(string host, EndpointBindingMode endpointBindingMode)
+    {
+        using var builder = TestDistributedApplicationBuilder.Create();
+
+        var tcs = new TaskCompletionSource();
+        var projectA = builder.AddProject<ProjectA>("projecta")
+            .WithHttpsEndpoint()
+            .WithEndpoint("https", e => e.TargetHost = host, createIfNotExists: false)
+            .OnBeforeResourceStarted((_, _, _) =>
+            {
+                tcs.SetResult();
+                return Task.CompletedTask;
+            });
+
+        var app = await builder.BuildAsync();
+        await app.StartAsync();
+        await tcs.Task;
+
+        var urls = projectA.Resource.Annotations.OfType<ResourceUrlAnnotation>();
+        Assert.Collection(urls,
+            url => Assert.StartsWith("https://localhost:", url.Url),
+            url => Assert.StartsWith($"https://{Environment.MachineName}:", url.Url));
+
+        EndpointAnnotation endpoint = Assert.Single(projectA.Resource.Annotations.OfType<EndpointAnnotation>());
+        Assert.NotNull(endpoint.AllocatedEndpoint);
+        Assert.Equal(endpointBindingMode, endpoint.AllocatedEndpoint.BindingMode);
+        Assert.Equal("localhost", endpoint.AllocatedEndpoint.Address);
+
+        await app.StopAsync();
+    }
+
     private sealed class TestProject : IProjectMetadata
     {
         public string ProjectPath => "projectpath";