diff --git a/src/mono/wasm/debugger/BrowserDebugProxy/MonoProxy.cs b/src/mono/wasm/debugger/BrowserDebugProxy/MonoProxy.cs
index 7d2245da67784a..0aa7650c42c2bd 100644
--- a/src/mono/wasm/debugger/BrowserDebugProxy/MonoProxy.cs
+++ b/src/mono/wasm/debugger/BrowserDebugProxy/MonoProxy.cs
@@ -1539,8 +1539,9 @@ protected async Task<DebugStore> RuntimeReady(SessionId sessionId, CancellationT
             ExecutionContext context = GetContext(sessionId);
             if (Interlocked.CompareExchange(ref context.ready, new TaskCompletionSource<DebugStore>(), null) != null)
                 return await context.ready.Task;
-
-            await context.SdbAgent.SendDebuggerAgentCommand(CmdEventRequest.ClearAllBreakpoints, null, token);
+            var res = await context.SdbAgent.SendDebuggerAgentCommand(CmdEventRequest.ClearAllBreakpoints, null, token, false);
+            if (res.HasError) //it's not a wasm page then the command returns an error
+                return null;
 
             if (context.PauseOnExceptions != PauseOnExceptionsKind.None && context.PauseOnExceptions != PauseOnExceptionsKind.Unset)
                 await context.SdbAgent.EnableExceptions(context.PauseOnExceptions, token);
diff --git a/src/mono/wasm/debugger/DebuggerTestSuite/BreakpointTests.cs b/src/mono/wasm/debugger/DebuggerTestSuite/BreakpointTests.cs
index cb21ab4e9f2257..7949ebec263fa6 100644
--- a/src/mono/wasm/debugger/DebuggerTestSuite/BreakpointTests.cs
+++ b/src/mono/wasm/debugger/DebuggerTestSuite/BreakpointTests.cs
@@ -470,8 +470,10 @@ await SendCommandAndCheck(null, "Debugger.resume",
                 });
         }
 
-        [ConditionalFact(nameof(RunningOnChrome))]
-        public async Task CreateGoodBreakpointAndHitGoToNonWasmPageComeBackAndHitAgain()
+        [ConditionalTheory(nameof(RunningOnChrome))]
+        [InlineData("load_non_wasm_page")]
+        [InlineData("load_non_wasm_page_forcing_runtime_ready")] //to simulate the same behavior that has when debugging from VS and OnDefaultContextCreated is called
+        public async Task CreateGoodBreakpointAndHitGoToNonWasmPageComeBackAndHitAgain(string func_name)
         {
             var bp = await SetBreakpoint("dotnet://debugger-test.dll/debugger-test.cs", 10, 8);
             var pause_location = await EvaluateAndCheck(
@@ -500,7 +502,7 @@ public async Task CreateGoodBreakpointAndHitGoToNonWasmPageComeBackAndHitAgain()
 
             var run_method = JObject.FromObject(new
             {
-                expression = "window.setTimeout(function() { load_non_wasm_page(); }, 1);"
+                expression = "window.setTimeout(function() { " + func_name + "(); }, 1);"
             });
             await cli.SendCommand("Runtime.evaluate", run_method, token);
             await Task.Delay(1000, token);
diff --git a/src/mono/wasm/debugger/tests/debugger-test/debugger-driver.html b/src/mono/wasm/debugger/tests/debugger-test/debugger-driver.html
index fdbbc640696ac3..b6522cf3cc79a8 100644
--- a/src/mono/wasm/debugger/tests/debugger-test/debugger-driver.html
+++ b/src/mono/wasm/debugger/tests/debugger-test/debugger-driver.html
@@ -92,6 +92,10 @@
 			console.log("load_wasm_page_without_assets")
 			window.location.replace("http://localhost:9400/wasm-page-without-assets.html");
 		}
+		function load_non_wasm_page_forcing_runtime_ready () {
+			console.log("load_non_wasm_page_forcing_runtime_ready")
+			window.location.replace("http://localhost:9400/non-wasm-page-forcing-runtime-ready.html");
+		}
 		</script>
 
 		<script type="text/javascript" src="other.js"></script>
diff --git a/src/mono/wasm/debugger/tests/debugger-test/debugger-test.csproj b/src/mono/wasm/debugger/tests/debugger-test/debugger-test.csproj
index 0ea4fcc719f4b8..0e457832913513 100644
--- a/src/mono/wasm/debugger/tests/debugger-test/debugger-test.csproj
+++ b/src/mono/wasm/debugger/tests/debugger-test/debugger-test.csproj
@@ -13,6 +13,7 @@
   <ItemGroup>
     <WasmExtraFilesToDeploy Include="debugger-driver.html" />
     <WasmExtraFilesToDeploy Include="non-wasm-page.html" />
+    <WasmExtraFilesToDeploy Include="non-wasm-page-forcing-runtime-ready.html" />
     <WasmExtraFilesToDeploy Include="wasm-page-without-assets.html" />
     <WasmExtraFilesToDeploy Include="other.js" />
     <WasmExtraFilesToDeploy Include="weather.json" />
diff --git a/src/mono/wasm/debugger/tests/debugger-test/non-wasm-page-forcing-runtime-ready.html b/src/mono/wasm/debugger/tests/debugger-test/non-wasm-page-forcing-runtime-ready.html
new file mode 100644
index 00000000000000..22ab25fb23040e
--- /dev/null
+++ b/src/mono/wasm/debugger/tests/debugger-test/non-wasm-page-forcing-runtime-ready.html
@@ -0,0 +1,14 @@
+<!doctype html>
+<html lang="en-us">
+	<head>
+	</head>
+	<body>
+	<script type='text/javascript'>
+		console.debug ("#debugger-app-ready#");
+		console.debug("mono_wasm_runtime_ready", "fe00e07a-5519-4dfe-b35a-f867dbaf2e28");
+		function reload_wasm_page () {
+			window.location.replace("http://localhost:9400/debugger-driver.html");
+		}
+	</script>
+	</body>
+</html>