diff --git a/lib/irb.rb b/lib/irb.rb
index c76c3f569..01f4c7697 100644
--- a/lib/irb.rb
+++ b/lib/irb.rb
@@ -77,6 +77,15 @@ class Irb
     PROMPT_MAIN_TRUNCATE_OMISSION = '...'
     CONTROL_CHARACTERS_PATTERN = "\x00-\x1F"
 
+    # Track the nesting depth of run loops. This is used for history management
+    # only the outermost run loop should load/save history.
+    @run_nesting_depth = 0
+
+    class << self
+      # TODO: When refactoring to v2.0, find a better way to manage and track nesting sessions.
+      attr_accessor :run_nesting_depth
+    end
+
     # Returns the current context of this irb session
     attr_reader :context
     # The lexer used by this irb session
@@ -148,7 +157,10 @@ def debug_readline(binding)
     end
 
     def run(conf = IRB.conf)
-      in_nested_session = !!conf[:MAIN_CONTEXT]
+      # Use run_nesting_depth to determine if we're in a nested session.
+      in_nested_session = Irb.run_nesting_depth > 0
+      Irb.run_nesting_depth += 1
+
       conf[:IRB_RC].call(context) if conf[:IRB_RC]
       prev_context = conf[:MAIN_CONTEXT]
       conf[:MAIN_CONTEXT] = context
@@ -174,6 +186,8 @@ def run(conf = IRB.conf)
           eval_input
         end
       ensure
+        Irb.run_nesting_depth -= 1
+
         # Do not restore to nil. It will cause IRB crash when used with threads.
         IRB.conf[:MAIN_CONTEXT] = prev_context if prev_context
 
diff --git a/test/irb/test_history.rb b/test/irb/test_history.rb
index 77b680d91..c6e931e80 100644
--- a/test/irb/test_history.rb
+++ b/test/irb/test_history.rb
@@ -565,6 +565,29 @@ def test_direct_debug_session_loads_history
       assert_include(output, "0: old_history_1")
     end
 
+    def test_history_saving_with_irb_start_after_debug_console_setup
+      # this makes debug.gem run activate_irb_integration, which sets up IRB context for debug.gem
+      @envs['RUBY_DEBUG_IRB_CONSOLE'] = "1"
+      write_history ""
+
+      write_ruby <<~'RUBY'
+        require 'debug' # this starts the debug.gem session, which runs activate_irb_integration
+        require 'irb'
+        puts 'binding.irb' # integration test uses binding.irb to identify the start of the IRB session
+        IRB.start
+      RUBY
+
+      run_ruby_file do
+        type "puts 'from_irb_start'"
+        type "exit"
+      end
+
+      assert_equal <<~HISTORY, @history_file.open.read
+        puts 'from_irb_start'
+        exit
+      HISTORY
+    end
+
     private
 
     def write_history(history)