diff --git a/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.cpp b/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.cpp
index f3614b08faa..5d9ddda55be 100644
--- a/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.cpp
+++ b/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.cpp
@@ -45,7 +45,7 @@ void HostAgent::handleRequest(const cdp::PreparsedRequest& req) {
   if (req.method == "Log.enable") {
     sessionState_.isLogDomainEnabled = true;
 
-    if (sessionState_.isFuseboxClientDetected) {
+    if (fuseboxClientType_ == FuseboxClientType::Fusebox) {
       sendFuseboxNotice();
     }
 
@@ -66,6 +66,14 @@ void HostAgent::handleRequest(const cdp::PreparsedRequest& req) {
   } else if (req.method == "Runtime.enable") {
     sessionState_.isRuntimeDomainEnabled = true;
 
+    if (fuseboxClientType_ == FuseboxClientType::Unknown) {
+      // Since we know the Fusebox frontend sends
+      // FuseboxClient.setClientMetadata before enabling the Runtime domain, we
+      // can conclude that we're dealing with some other client.
+      fuseboxClientType_ = FuseboxClientType::NonFusebox;
+      sendNonFuseboxNotice();
+    }
+
     shouldSendOKResponse = true;
     isFinishedHandlingRequest = false;
   } else if (req.method == "Runtime.disable") {
@@ -100,7 +108,7 @@ void HostAgent::handleRequest(const cdp::PreparsedRequest& req) {
     shouldSendOKResponse = true;
     isFinishedHandlingRequest = true;
   } else if (req.method == "FuseboxClient.setClientMetadata") {
-    sessionState_.isFuseboxClientDetected = true;
+    fuseboxClientType_ = FuseboxClientType::Fusebox;
 
     if (sessionState_.isLogDomainEnabled) {
       sendFuseboxNotice();
@@ -136,6 +144,18 @@ void HostAgent::sendFuseboxNotice() {
       kFuseboxNotice, {"font-family: sans-serif;", "font-family: monospace;"});
 }
 
+void HostAgent::sendNonFuseboxNotice() {
+  static constexpr auto kNonFuseboxNotice =
+      ANSI_COLOR_BG_YELLOW ANSI_WEIGHT_BOLD
+      "NOTE: " ANSI_WEIGHT_RESET
+      "You are using an unsupported debugging client. "
+      "Use the Dev Menu in your app (or type `j` in the Metro terminal) to open the latest, supported React Native debugger."sv;
+
+  std::vector<std::string> args;
+  args.emplace_back(kNonFuseboxNotice);
+  sendConsoleMessage({ConsoleAPIType::kInfo, args});
+}
+
 void HostAgent::sendInfoLogEntry(
     std::string_view text,
     std::initializer_list<std::string_view> args) {
diff --git a/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.h b/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.h
index 6a4f8fe6f39..363339fac6d 100644
--- a/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.h
+++ b/packages/react-native/ReactCommon/jsinspector-modern/HostAgent.h
@@ -62,6 +62,8 @@ class HostAgent final {
   void setCurrentInstanceAgent(std::shared_ptr<InstanceAgent> agent);
 
  private:
+  enum class FuseboxClientType { Unknown, Fusebox, NonFusebox };
+
   /**
    * Send a simple Log.entryAdded notification with the given
    * \param text. You must ensure that the frontend has enabled Log
@@ -76,6 +78,7 @@ class HostAgent final {
       std::initializer_list<std::string_view> args = {});
 
   void sendFuseboxNotice();
+  void sendNonFuseboxNotice();
 
   /**
    * Send a console message to the frontend, or buffer it to be sent later.
@@ -86,6 +89,7 @@ class HostAgent final {
   HostTargetController& targetController_;
   const HostTarget::SessionMetadata sessionMetadata_;
   std::shared_ptr<InstanceAgent> instanceAgent_;
+  FuseboxClientType fuseboxClientType_{FuseboxClientType::Unknown};
 
   /**
    * A shared reference to the session's state. This is only safe to access
diff --git a/packages/react-native/ReactCommon/jsinspector-modern/SessionState.h b/packages/react-native/ReactCommon/jsinspector-modern/SessionState.h
index 69a75c5b7a7..36c4c72666f 100644
--- a/packages/react-native/ReactCommon/jsinspector-modern/SessionState.h
+++ b/packages/react-native/ReactCommon/jsinspector-modern/SessionState.h
@@ -36,8 +36,6 @@ struct SessionState {
   std::unordered_map<std::string, ExecutionContextSelectorSet>
       subscribedBindings;
 
-  bool isFuseboxClientDetected{false};
-
   /**
    * Messages logged through the HostAgent::sendConsoleMessage and
    * InstanceAgent::sendConsoleMessage utilities that have not yet been sent to