diff --git a/src/mono/wasm/debugger/BrowserDebugHost/DebugProxyHost.cs b/src/mono/wasm/debugger/BrowserDebugHost/DebugProxyHost.cs
index b97ffe7ef0fc7..9129c61c9c308 100644
--- a/src/mono/wasm/debugger/BrowserDebugHost/DebugProxyHost.cs
+++ b/src/mono/wasm/debugger/BrowserDebugHost/DebugProxyHost.cs
@@ -24,7 +24,7 @@ public static async Task RunDebugProxyAsync(ProxyOptions options, string[] args,
         {
             RunDevToolsProxyAsync(options, args, loggerFactory, token)
         };
-        if (!options.RunningForBlazor)
+        if (!options.RunningForBlazor || options.IsFirefoxDebugging)
             tasks.Add(RunFirefoxServerLoopAsync(options, args, loggerFactory, token));
 
         Task completedTask = await Task.WhenAny(tasks);
diff --git a/src/mono/wasm/debugger/BrowserDebugProxy/Firefox/FirefoxDebuggerProxy.cs b/src/mono/wasm/debugger/BrowserDebugProxy/Firefox/FirefoxDebuggerProxy.cs
index 6824ff3811093..57a590af6badb 100644
--- a/src/mono/wasm/debugger/BrowserDebugProxy/Firefox/FirefoxDebuggerProxy.cs
+++ b/src/mono/wasm/debugger/BrowserDebugProxy/Firefox/FirefoxDebuggerProxy.cs
@@ -5,7 +5,9 @@
 
 using System;
 using System.Diagnostics.CodeAnalysis;
+using System.Linq;
 using System.Net;
+using System.Net.NetworkInformation;
 using System.Net.Sockets;
 using System.Threading;
 using System.Threading.Tasks;
@@ -26,10 +28,17 @@ public static void StartListener(int proxyPort, ILogger logger, int browserPort
     {
         if (s_tcpListener is null)
         {
+            // If there is an existing listener on @proxyPort, then use a new dynamic port.
+            // Blazor always tries to open the same port (specified in @proxyPort) to avoid
+            // creating a lot of remote debugging connections on firefox
+            if (proxyPort != 0 && IPGlobalProperties.GetIPGlobalProperties().GetActiveTcpListeners().Any(x => x.Port == proxyPort))
+            {
+                proxyPort = 0;
+            }
             s_tcpListener = new TcpListener(IPAddress.Parse("127.0.0.1"), proxyPort);
             s_tcpListener.Start();
             Console.WriteLine($"Debug proxy for firefox now listening on tcp://{s_tcpListener.LocalEndpoint}." +
-                                (browserPort >= 0 ? $" And expecting firefox at port {browserPort} ." : string.Empty));
+                                (browserPort >= 0 ? $" And expecting firefox at port {browserPort}." : string.Empty));
         }
     }
 
diff --git a/src/mono/wasm/debugger/BrowserDebugProxy/ProxyOptions.cs b/src/mono/wasm/debugger/BrowserDebugProxy/ProxyOptions.cs
index ca8084795b114..0fdfdfc8a8e01 100644
--- a/src/mono/wasm/debugger/BrowserDebugProxy/ProxyOptions.cs
+++ b/src/mono/wasm/debugger/BrowserDebugProxy/ProxyOptions.cs
@@ -28,4 +28,5 @@ public int DevToolsDebugPort
     }
     public string? LogPath { get; set; }
     public bool RunningForBlazor { get; set; }
+    public bool IsFirefoxDebugging { get; set; }
 }