diff --git a/lib/irb/context.rb b/lib/irb/context.rb
index fafe99d57..668a823f5 100644
--- a/lib/irb/context.rb
+++ b/lib/irb/context.rb
@@ -649,6 +649,21 @@ def parse_command(code)
       end
     end
 
+    def colorize_input(input, complete:)
+      if IRB.conf[:USE_COLORIZE] && IRB::Color.colorable?
+        lvars = local_variables || []
+        if parse_command(input)
+          name, sep, arg = input.split(/(\s+)/, 2)
+          arg = IRB::Color.colorize_code(arg, complete: complete, local_variables: lvars)
+          "#{IRB::Color.colorize(name, [:BOLD])}\e[m#{sep}#{arg}"
+        else
+          IRB::Color.colorize_code(input, complete: complete, local_variables: lvars)
+        end
+      else
+        Reline::Unicode.escape_for_print(input)
+      end
+    end
+
     def inspect_last_value # :nodoc:
       @inspect_method.inspect_value(@last_value)
     end
diff --git a/lib/irb/debug.rb b/lib/irb/debug.rb
index 1ec2335a8..cd64b77ad 100644
--- a/lib/irb/debug.rb
+++ b/lib/irb/debug.rb
@@ -57,22 +57,18 @@ def DEBUGGER__.capture_frames(*args)
           DEBUGGER__::ThreadClient.prepend(SkipPathHelperForIRB)
         end
 
-        if !@output_modifier_defined && !DEBUGGER__::CONFIG[:no_hint]
-          irb_output_modifier_proc = Reline.output_modifier_proc
-
-          Reline.output_modifier_proc = proc do |output, complete:|
-            unless output.strip.empty?
-              cmd = output.split(/\s/, 2).first
+        if !DEBUGGER__::CONFIG[:no_hint] && irb.context.io.is_a?(RelineInputMethod)
+          Reline.output_modifier_proc = proc do |input, complete:|
+            unless input.strip.empty?
+              cmd = input.split(/\s/, 2).first
 
               if !complete && DEBUGGER__.commands.key?(cmd)
-                output = output.sub(/\n$/, " # debug command\n")
+                input = input.sub(/\n$/, " # debug command\n")
               end
             end
 
-            irb_output_modifier_proc.call(output, complete: complete)
+            irb.context.colorize_input(input, complete: complete)
           end
-
-          @output_modifier_defined = true
         end
 
         true
diff --git a/lib/irb/input-method.rb b/lib/irb/input-method.rb
index 82c1e7329..210d3da78 100644
--- a/lib/irb/input-method.rb
+++ b/lib/irb/input-method.rb
@@ -265,24 +265,9 @@ def initialize(completor)
         @completion_params = [preposing, target, postposing, bind]
         @completor.completion_candidates(preposing, target, postposing, bind: bind)
       }
-      Reline.output_modifier_proc =
-        if IRB.conf[:USE_COLORIZE]
-          proc do |output, complete: |
-            next unless IRB::Color.colorable?
-            lvars = IRB.CurrentContext&.local_variables || []
-            if IRB.CurrentContext&.parse_command(output)
-              name, sep, arg = output.split(/(\s+)/, 2)
-              arg = IRB::Color.colorize_code(arg, complete: complete, local_variables: lvars)
-              "#{IRB::Color.colorize(name, [:BOLD])}\e[m#{sep}#{arg}"
-            else
-              IRB::Color.colorize_code(output, complete: complete, local_variables: lvars)
-            end
-          end
-        else
-          proc do |output|
-            Reline::Unicode.escape_for_print(output)
-          end
-        end
+      Reline.output_modifier_proc = proc do |input, complete:|
+        IRB.CurrentContext.colorize_input(input, complete: complete)
+      end
       Reline.dig_perfect_match_proc = ->(matched) { display_document(matched) }
       Reline.autocompletion = IRB.conf[:USE_AUTOCOMPLETE]
 
diff --git a/test/irb/yamatanooroti/test_rendering.rb b/test/irb/yamatanooroti/test_rendering.rb
index 44e07a3a1..834c501d5 100644
--- a/test/irb/yamatanooroti/test_rendering.rb
+++ b/test/irb/yamatanooroti/test_rendering.rb
@@ -507,6 +507,28 @@ def test_debug_integration_doesnt_hint_non_debugger_commands
     File.unlink(script) if script
   end
 
+  def test_debug_integration_doesnt_hint_debugger_commands_in_nomultiline_mode
+    write_irbrc <<~'LINES'
+      IRB.conf[:USE_SINGLELINE] = true
+    LINES
+    script = Tempfile.create(["debug", ".rb"])
+    script.write <<~RUBY
+      puts 'start IRB'
+      binding.irb
+    RUBY
+    script.close
+    start_terminal(40, 80, %W{ruby -I#{@pwd}/lib #{script.to_path}}, startup_message: 'start IRB')
+    write("debug\n")
+    write("pp 1")
+    close
+
+    screen = result.join("\n").sub(/\n*\z/, "\n")
+    # submitted input shouldn't contain hint
+    assert_include(screen, "irb:rdbg(main):002> pp 1\n")
+  ensure
+    File.unlink(script) if script
+  end
+
   private
 
   def write_irbrc(content)