diff --git a/app_check/src/desktop/debug_provider_desktop.cc b/app_check/src/desktop/debug_provider_desktop.cc
index e7658ee371..dcccc47f1e 100644
--- a/app_check/src/desktop/debug_provider_desktop.cc
+++ b/app_check/src/desktop/debug_provider_desktop.cc
@@ -15,8 +15,11 @@
 #include "app_check/src/desktop/debug_provider_desktop.h"
 
 #include <cstdint>
+#include <cstdio>
+#include <cstdlib>
 #include <map>
 #include <memory>
+#include <mutex>
 #include <string>
 #include <utility>
 
@@ -26,6 +29,7 @@
 #include "app/rest/util.h"
 #include "app/src/log.h"
 #include "app/src/scheduler.h"
+#include "app/src/uuid.h"
 #include "app_check/src/desktop/debug_token_request.h"
 #include "app_check/src/desktop/token_response.h"
 #include "firebase/app_check/debug_provider.h"
@@ -34,6 +38,22 @@ namespace firebase {
 namespace app_check {
 namespace internal {
 
+namespace {
+std::string GenerateUuidString() {
+  firebase::internal::Uuid uuid;
+  uuid.Generate();
+  char uuid_str[37];
+  snprintf(
+      uuid_str, sizeof(uuid_str),
+      "%02x%02x%02x%02x-%02x%02x-%02x%02x-%02x%02x-%02x%02x%02x%02x%02x%02x",
+      uuid.data[0], uuid.data[1], uuid.data[2], uuid.data[3], uuid.data[4],
+      uuid.data[5], uuid.data[6], uuid.data[7], uuid.data[8], uuid.data[9],
+      uuid.data[10], uuid.data[11], uuid.data[12], uuid.data[13], uuid.data[14],
+      uuid.data[15]);
+  return std::string(uuid_str);
+}
+}  // namespace
+
 class DebugAppCheckProvider : public AppCheckProvider {
  public:
   DebugAppCheckProvider(App* app, const std::string& token);
@@ -115,23 +135,56 @@ void DebugAppCheckProvider::GetTokenInternal(
     bool limited_use,
     std::function<void(AppCheckToken, int, const std::string&)>
         completion_callback) {
-  // Identify the user's debug token
-  const char* debug_token_cstr;
-  if (!debug_token_.empty()) {
-    debug_token_cstr = debug_token_.c_str();
-  } else {
-    debug_token_cstr = std::getenv("APP_CHECK_DEBUG_TOKEN");
+  static std::mutex token_mutex;
+  static bool logged_token = false;
+  std::string message_to_log;
+
+  {
+    std::lock_guard<std::mutex> lock(token_mutex);
+    if (debug_token_.empty()) {
+      if (const char* env_token = std::getenv("APP_CHECK_DEBUG_TOKEN")) {
+        debug_token_ = env_token;
+      } else {
+        debug_token_ = GenerateUuidString();
+      }
+    }
+
+    if (!logged_token && !debug_token_.empty()) {
+      logged_token = true;
+      std::string app_id = app_->options().app_id();
+      std::string project_id = app_->options().project_id();
+      message_to_log =
+          std::string("\nWARNING: Firebase App Check debug token: ") +
+          debug_token_ + "\n\n" +
+          "To use this token for app debugging, register it with your "
+          "project.\n\n" +
+          "You can do so in the Firebase Console: \n" +
+          "https://console.firebase.google.com/project/" + project_id +
+          "/appcheck/apps?selectedAppId=" + app_id + " \n\n" +
+          "Or using the Firebase CLI: \n" +
+          "firebase appcheck:debugtokens:create " + debug_token_ + " --app " +
+          app_id + "\n\n" +
+          "Note: To keep your project secure, please revoke and delete this "
+          "token using the \n" +
+          "Firebase Console or the CLI (`firebase "
+          "appcheck:debugtokens:delete`) "
+          "when you finish debugging.\n\n" +
+          "Warning: This debug token is a secret and should not be shared or "
+          "uploaded to source code.\n\n" +
+          "Debug Token Guide: "
+          "https://firebase.google.com/docs/app-check/ios/debug-provider\n" +
+          "Firebase CLI install instructions: "
+          "https://firebase.google.com/docs/cli\n";
+    }
   }
 
-  if (!debug_token_cstr) {
-    completion_callback({}, kAppCheckErrorInvalidConfiguration,
-                        "Missing debug token");
-    return;
+  if (!message_to_log.empty()) {
+    firebase::LogWarning("%s", message_to_log.c_str());
   }
 
   // Exchange debug token with the backend to get a proper attestation token.
   auto request = std::make_shared<DebugTokenRequest>(app_);
-  request->SetDebugToken(debug_token_cstr);
+  request->SetDebugToken(debug_token_);
   request->SetLimitedUse(limited_use);
 
   // Use an async call, since we don't want to block on the server response.
diff --git a/release_build_files/readme.md b/release_build_files/readme.md
index 2fef1d63ac..854766d082 100644
--- a/release_build_files/readme.md
+++ b/release_build_files/readme.md
@@ -615,6 +615,7 @@ code.
 ## Release Notes
 ### Upcoming
 - Changes
+    - App Check (Desktop): The App Check Debug Provider will now automatically generate a local debug token if one isn't provided, and print instructions for registering it via the Firebase Console or CLI.
     - General (iOS): Fixed an issue where prebuilt iOS/tvOS frameworks had an incorrect minimum deployment target (minos), which caused linker warnings.
     - Auth (Desktop): Fixed log spam and high CPU utilization when offline by moving `USE_AUTH_EMULATOR` environment variable check to initialization and eliminating per-request logging (#1629).
     - Messaging: Added new Registration methods using Installation Ids.