diff --git a/lib/debug/config.rb b/lib/debug/config.rb
index ab4c9c559..eb132ce4a 100644
--- a/lib/debug/config.rb
+++ b/lib/debug/config.rb
@@ -158,6 +158,26 @@ def update conf
           SESSION.set_no_sigint_hook old, new
         end
       end
+
+      if_updated old_conf, conf, :irb_console do |old, new|
+        if defined?(SESSION) && SESSION.active?
+          # irb_console is switched from true to false
+          if old
+            Reline.completion_proc = nil
+            Reline.output_modifier_proc = nil
+            Reline.autocompletion = false
+            Reline.dig_perfect_match_proc = nil
+            SESSION.reset_ui UI_LocalConsole.new
+          # irb_console is switched from false to true
+          else
+            if CONFIG[:open]
+              SESSION.instance_variable_get(:@ui).puts "\nIRB is not supported on the remote console."
+            else
+              SESSION.activate_irb_integration
+            end
+          end
+        end
+      end
     end
 
     private def if_updated old_conf, new_conf, key
diff --git a/lib/debug/session.rb b/lib/debug/session.rb
index c5b410182..05dc7f508 100644
--- a/lib/debug/session.rb
+++ b/lib/debug/session.rb
@@ -202,11 +202,6 @@ def activate ui = nil, on_fork: false
         end
         @tp_thread_end.enable
 
-        if CONFIG[:irb_console] && !CONFIG[:open]
-          require_relative "irb_integration"
-          thc.activate_irb_integration
-        end
-
         # session start
         q << true
         session_server_main
@@ -214,6 +209,12 @@ def activate ui = nil, on_fork: false
       first_q << :ok
 
       q.pop
+
+      # For activating irb:rdbg with startup config like `RUBY_DEBUG_IRB_CONSOLE=1`
+      # Because in that case the `Config#if_updated` callback would not be triggered
+      if CONFIG[:irb_console] && !CONFIG[:open]
+        activate_irb_integration
+      end
     end
 
     def deactivate
@@ -942,10 +943,11 @@ def register_default_command
       register_command 'irb' do |arg|
         if @ui.remote?
           @ui.puts "\nIRB is not supported on the remote console."
-          :retry
         else
-          request_eval :irb, nil
+          config_set :irb_console, true
         end
+
+        :retry
       end
 
       ### Trace
@@ -1876,6 +1878,12 @@ def check_unsafe
       end
     end
 
+    def activate_irb_integration
+      require_relative "irb_integration"
+      thc = get_thread_client(@session_server)
+      thc.activate_irb_integration
+    end
+
     def enter_postmortem_session exc
       return unless exc.instance_variable_defined? :@__debugger_postmortem_frames
 
diff --git a/lib/debug/thread_client.rb b/lib/debug/thread_client.rb
index 753898560..e10d4d97f 100644
--- a/lib/debug/thread_client.rb
+++ b/lib/debug/thread_client.rb
@@ -1056,9 +1056,6 @@ def wait_next_action_
             end
           when :call
             result = frame_eval(eval_src)
-          when :irb
-            require_relative "irb_integration"
-            activate_irb_integration
           when :display, :try_display
             failed_results = []
             eval_src.each_with_index{|src, i|
diff --git a/test/console/irb_test.rb b/test/console/irb_test.rb
index 478a37036..515a240c7 100644
--- a/test/console/irb_test.rb
+++ b/test/console/irb_test.rb
@@ -4,15 +4,6 @@
 
 module DEBUGGER__
   class IrbTest < ConsoleTestCase
-    def setup
-      @original_pager = ENV["PAGER"]
-      ENV["PAGER"] = "cat"
-    end
-
-    def teardown
-      ENV["PAGER"] = @original_pager
-    end
-
     def program
       <<~RUBY
       1| a = 1
@@ -26,6 +17,12 @@ def test_irb_command_is_disabled_in_remote_mode
         assert_line_text 'IRB is not supported on the remote console.'
         type 'q!'
       end
+
+      debug_code(program, remote: :remote_only) do
+        type 'config set irb_console true'
+        assert_line_text 'IRB is not supported on the remote console.'
+        type 'q!'
+      end
     end
 
     def test_irb_command_switches_console_to_irb
@@ -38,6 +35,11 @@ def test_irb_command_switches_console_to_irb
         type 'next'
         type 'info'
         assert_line_text([/a = 1/, /b = nil/])
+
+        # disable irb console
+        type 'config set irb_console false'
+        type '456'
+        assert_raw_line_text '(rdbg) 456'
         type 'q!'
       end
     end
@@ -53,10 +55,25 @@ def test_irb_console_config_activates_irb
         type 'next'
         type 'info'
         assert_line_text([/a = 1/, /b = nil/])
+
+        # disable irb console
+        type 'config set irb_console false'
+        type '456'
+        assert_raw_line_text '(rdbg) 456'
         type 'q!'
       end
     ensure
       ENV["RUBY_DEBUG_IRB_CONSOLE"] = nil
     end
+
+    private
+
+    # assert_line_text ignores the prompt line, so we can't use it to assert the prompt transition
+    # assert_raw_line_text is a workaround for that
+    def assert_raw_line_text(expectation)
+      @scenario.push(Proc.new do |test_info|
+        assert_include(test_info.last_backlog.join, expectation)
+      end)
+    end
   end
 end