diff --git a/src/mono/wasm/host/WebServer.cs b/src/mono/wasm/host/WebServer.cs
index aed1948470334c..1f448edcb98eab 100644
--- a/src/mono/wasm/host/WebServer.cs
+++ b/src/mono/wasm/host/WebServer.cs
@@ -1,13 +1,9 @@
 // Licensed to the .NET Foundation under one or more agreements.
 // The .NET Foundation licenses this file to you under the MIT license.
 
-using System;
-using System.Collections.Generic;
-using System.Linq;
 using System.Threading;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Hosting;
-using Microsoft.AspNetCore.Hosting.Server.Features;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.Extensions.Logging;
 using Microsoft.Extensions.Options;
@@ -21,6 +17,7 @@ public class WebServer
     internal static async Task<(ServerURLs, IWebHost)> StartAsync(WebServerOptions options, ILogger logger, CancellationToken token)
     {
         string[] urls = options.Urls;
+        TaskCompletionSource<ServerURLs> realUrlsAvailableTcs = new();
 
         IWebHostBuilder builder = new WebHostBuilder()
             .UseKestrel()
@@ -43,6 +40,7 @@ public class WebServer
                 }
                 services.AddSingleton(logger);
                 services.AddSingleton(Options.Create(options));
+                services.AddSingleton(realUrlsAvailableTcs);
                 services.AddRouting();
             })
             .UseUrls(urls);
@@ -53,27 +51,11 @@ public class WebServer
         IWebHost? host = builder.Build();
         await host.StartAsync(token);
 
-        ICollection<string>? addresses = host.ServerFeatures
-                            .Get<IServerAddressesFeature>()?
-                            .Addresses;
+        if (token.CanBeCanceled)
+            token.Register(async () => await host.StopAsync());
 
-        string? ipAddress =
-                        addresses?
-                        .Where(a => a.StartsWith("http:", StringComparison.InvariantCultureIgnoreCase))
-                        .Select(a => new Uri(a))
-                        .Select(uri => uri.ToString())
-                        .FirstOrDefault();
-
-        string? ipAddressSecure =
-                        addresses?
-                        .Where(a => a.StartsWith("https:", StringComparison.OrdinalIgnoreCase))
-                        .Select(a => new Uri(a))
-                        .Select(uri => uri.ToString())
-                        .FirstOrDefault();
-
-        return ipAddress == null || ipAddressSecure == null
-            ? throw new InvalidOperationException("Failed to determine web server's IP address or port")
-            : (new ServerURLs(ipAddress, ipAddressSecure), host);
+        ServerURLs serverUrls = await realUrlsAvailableTcs.Task;
+        return (serverUrls, host);
     }
 
 }
diff --git a/src/mono/wasm/host/WebServerStartup.cs b/src/mono/wasm/host/WebServerStartup.cs
index e09cdd61963fb2..933eeb6b6fc196 100644
--- a/src/mono/wasm/host/WebServerStartup.cs
+++ b/src/mono/wasm/host/WebServerStartup.cs
@@ -7,15 +7,19 @@
 using System.IO;
 using System.Net;
 using System.Net.WebSockets;
+using System.Linq;
 using System.Reflection;
 using System.Runtime.InteropServices;
 using System.Threading.Tasks;
 using System.Web;
 using Microsoft.AspNetCore.Builder;
 using Microsoft.AspNetCore.Hosting;
+using Microsoft.AspNetCore.Hosting.Server.Features;
 using Microsoft.AspNetCore.Routing;
 using Microsoft.AspNetCore.StaticFiles;
 using Microsoft.Extensions.FileProviders;
+using Microsoft.Extensions.Hosting;
+using Microsoft.Extensions.Logging;
 using Microsoft.Extensions.Options;
 using Microsoft.WebAssembly.Diagnostics;
 
@@ -28,6 +32,8 @@ internal sealed class WebServerStartup
     private readonly IWebHostEnvironment _hostingEnvironment;
     private static readonly object LaunchLock = new object();
     private static string LaunchedDebugProxyUrl = "";
+    private ILogger? _logger;
+
     public WebServerStartup(IWebHostEnvironment hostingEnvironment) => _hostingEnvironment = hostingEnvironment;
 
     public static int StartDebugProxy(string devToolsHost)
@@ -52,8 +58,13 @@ public static int StartDebugProxy(string devToolsHost)
         return generateRandomPort;
     }
 
-    public void Configure(IApplicationBuilder app, IOptions<WebServerOptions> optionsContainer)
+    public void Configure(IApplicationBuilder app,
+                          IOptions<WebServerOptions> optionsContainer,
+                          TaskCompletionSource<ServerURLs> realUrlsAvailableTcs,
+                          ILogger logger,
+                          IHostApplicationLifetime applicationLifetime)
     {
+        _logger = logger;
         var provider = new FileExtensionContentTypeProvider();
         provider.Mappings[".wasm"] = "application/wasm";
         provider.Mappings[".cjs"] = "text/javascript";
@@ -144,5 +155,41 @@ public void Configure(IApplicationBuilder app, IOptions<WebServerOptions> option
                 return Task.CompletedTask;
             });
         });
+
+        applicationLifetime.ApplicationStarted.Register(() =>
+        {
+            try
+            {
+                ICollection<string>? addresses = app.ServerFeatures
+                                                    .Get<IServerAddressesFeature>()
+                                                    ?.Addresses;
+
+                string? ipAddress = null;
+                string? ipAddressSecure = null;
+                if (addresses is not null)
+                {
+                    ipAddress = GetHttpServerAddress(addresses, secure: false);
+                    ipAddressSecure = GetHttpServerAddress(addresses, secure: true);
+                }
+
+                if (ipAddress == null)
+                    realUrlsAvailableTcs.SetException(new InvalidOperationException("Failed to determine web server's IP address or port"));
+                else
+                    realUrlsAvailableTcs.SetResult(new ServerURLs(ipAddress, ipAddressSecure));
+            }
+            catch (Exception ex)
+            {
+                _logger?.LogError($"Failed to get urls for the webserver: {ex}");
+                realUrlsAvailableTcs.TrySetException(ex);
+                throw;
+            }
+
+            static string? GetHttpServerAddress(ICollection<string> addresses, bool secure)
+                => addresses?
+                        .Where(a => a.StartsWith(secure ? "https:" : "http:", StringComparison.InvariantCultureIgnoreCase))
+                        .Select(a => new Uri(a))
+                        .Select(uri => uri.ToString())
+                        .FirstOrDefault();
+        });
     }
 }