diff --git a/lib/irb/cmd/irb_info.rb b/lib/irb/cmd/irb_info.rb
index 5b905a09b..3abcc2435 100644
--- a/lib/irb/cmd/irb_info.rb
+++ b/lib/irb/cmd/irb_info.rb
@@ -15,7 +15,10 @@ def execute
         str += "IRB version: #{IRB.version}\n"
         str += "InputMethod: #{IRB.CurrentContext.io.inspect}\n"
         str += "Completion: #{IRB.CurrentContext.io.respond_to?(:completion_info) ? IRB.CurrentContext.io.completion_info : 'off'}\n"
-        str += ".irbrc path: #{IRB.rc_file}\n" if File.exist?(IRB.rc_file)
+        rc_files = IRB.rc_files.each_with_object([]) do |rc, files|
+          files << rc if File.exist?(rc)
+        end
+        str += ".irbrc paths: #{rc_files.join(", ")}\n" if rc_files.any?
         str += "RUBY_PLATFORM: #{RUBY_PLATFORM}\n"
         str += "LANG env: #{ENV["LANG"]}\n" if ENV["LANG"] && !ENV["LANG"].empty?
         str += "LC_ALL env: #{ENV["LC_ALL"]}\n" if ENV["LC_ALL"] && !ENV["LC_ALL"].empty?
diff --git a/lib/irb/history.rb b/lib/irb/history.rb
index 50fe1ce22..e1520bf86 100644
--- a/lib/irb/history.rb
+++ b/lib/irb/history.rb
@@ -14,7 +14,7 @@ def load_history
       if history_file = IRB.conf[:HISTORY_FILE]
         history_file = File.expand_path(history_file)
       end
-      history_file = IRB.rc_file("_history") unless history_file
+      history_file = IRB.rc_files("_history").first unless history_file
       if File.exist?(history_file)
         File.open(history_file, "r:#{IRB.conf[:LC_MESSAGES].encoding}") do |f|
           f.each { |l|
@@ -39,7 +39,7 @@ def save_history
         if history_file = IRB.conf[:HISTORY_FILE]
           history_file = File.expand_path(history_file)
         end
-        history_file = IRB.rc_file("_history") unless history_file
+        history_file = IRB.rc_files("_history").first unless history_file
 
         # Change the permission of a file that already exists[BUG #7694]
         begin
diff --git a/lib/irb/init.rb b/lib/irb/init.rb
index 66e7b6146..97fd12dbb 100644
--- a/lib/irb/init.rb
+++ b/lib/irb/init.rb
@@ -392,33 +392,41 @@ def IRB.parse_opts(argv: ::ARGV)
   # Run the config file
   def IRB.run_config
     if @CONF[:RC]
-      begin
-        file = rc_file
+      rc_files.each do |rc|
         # Because rc_file always returns `HOME/.irbrc` even if no rc file is present, we can't warn users about missing rc files.
         # Otherwise, it'd be very noisy.
-        load file if File.exist?(file)
+        load rc if File.exist?(rc)
       rescue StandardError, ScriptError => e
-        warn "Error loading RC file '#{file}':\n#{e.full_message(highlight: false)}"
+        warn "Error loading RC file '#{rc}':\n#{e.full_message(highlight: false)}"
       end
     end
   end
 
   IRBRC_EXT = "rc"
   def IRB.rc_file(ext = IRBRC_EXT)
+    warn "rc_file is deprecated, please use rc_files instead."
+    rc_files(ext).first
+  end
+
+  def IRB.rc_files(ext = IRBRC_EXT)
     if !@CONF[:RC_NAME_GENERATOR]
+      @CONF[:RC_NAME_GENERATOR] ||= []
+      existing_rc_files = []
+
       rc_file_generators do |rcgen|
-        @CONF[:RC_NAME_GENERATOR] ||= rcgen
-        if File.exist?(rcgen.call(IRBRC_EXT))
-          @CONF[:RC_NAME_GENERATOR] = rcgen
-          break
-        end
+        @CONF[:RC_NAME_GENERATOR] << rcgen
+        existing_rc_files << rcgen if File.exist?(rcgen.call(IRBRC_EXT))
+      end
+
+      if existing_rc_files.any?
+        @CONF[:RC_NAME_GENERATOR] = existing_rc_files
       end
     end
-    case rc_file = @CONF[:RC_NAME_GENERATOR].call(ext)
-    when String
+
+    @CONF[:RC_NAME_GENERATOR].map do |rc|
+      rc_file = rc.call(ext)
+      fail IllegalRCNameGenerator unless rc_file.is_a?(String)
       rc_file
-    else
-      fail IllegalRCNameGenerator
     end
   end
 
diff --git a/test/irb/test_cmd.rb b/test/irb/test_cmd.rb
index d99ac05c5..9270e86ec 100644
--- a/test/irb/test_cmd.rb
+++ b/test/irb/test_cmd.rb
@@ -77,6 +77,7 @@ def teardown
     def test_irb_info_multiline
       FileUtils.touch("#{@tmpdir}/.inputrc")
       FileUtils.touch("#{@tmpdir}/.irbrc")
+      FileUtils.touch("#{@tmpdir}/_irbrc")
 
       out, err = execute_lines(
         "irb_info",
@@ -88,7 +89,7 @@ def test_irb_info_multiline
         IRB\sversion:\sirb\s.+\n
         InputMethod:\sAbstract\sInputMethod\n
         Completion: .+\n
-        \.irbrc\spath:\s.+\n
+        \.irbrc\spaths:.*\.irbrc.*_irbrc\n
         RUBY_PLATFORM:\s.+\n
         East\sAsian\sAmbiguous\sWidth:\s\d\n
         #{@is_win ? 'Code\spage:\s\d+\n' : ''}
@@ -112,7 +113,7 @@ def test_irb_info_singleline
         IRB\sversion:\sirb\s.+\n
         InputMethod:\sAbstract\sInputMethod\n
         Completion: .+\n
-        \.irbrc\spath:\s.+\n
+        \.irbrc\spaths:\s.+\n
         RUBY_PLATFORM:\s.+\n
         East\sAsian\sAmbiguous\sWidth:\s\d\n
         #{@is_win ? 'Code\spage:\s\d+\n' : ''}
@@ -198,7 +199,7 @@ def test_irb_info_lang
         IRB\sversion:\sirb .+\n
         InputMethod:\sAbstract\sInputMethod\n
         Completion: .+\n
-        \.irbrc\spath: .+\n
+        \.irbrc\spaths: .+\n
         RUBY_PLATFORM: .+\n
         LANG\senv:\sja_JP\.UTF-8\n
         LC_ALL\senv:\sen_US\.UTF-8\n
diff --git a/test/irb/test_history.rb b/test/irb/test_history.rb
index f7ba2b9d3..22d04762c 100644
--- a/test/irb/test_history.rb
+++ b/test/irb/test_history.rb
@@ -136,7 +136,7 @@ def test_history_concurrent_use_not_present
         io.class::HISTORY << 'line1'
         io.class::HISTORY << 'line2'
 
-        history_file = IRB.rc_file("_history")
+        history_file = IRB.rc_files("_history").first
         assert_not_send [File, :file?, history_file]
         File.write(history_file, "line0\n")
         io.save_history
@@ -204,9 +204,10 @@ def assert_history(expected_history, initial_irb_history, input, input_method =
       backup_xdg_config_home = ENV.delete("XDG_CONFIG_HOME")
       IRB.conf[:LC_MESSAGES] = locale
       actual_history = nil
+      history_file = IRB.rc_files("_history").first
       Dir.mktmpdir("test_irb_history_") do |tmpdir|
         ENV["HOME"] = tmpdir
-        File.open(IRB.rc_file("_history"), "w") do |f|
+        File.open(history_file, "w") do |f|
           f.write(initial_irb_history)
         end
 
@@ -216,7 +217,7 @@ def assert_history(expected_history, initial_irb_history, input, input_method =
         if block_given?
           previous_history = []
           io.class::HISTORY.each { |line| previous_history << line }
-          yield IRB.rc_file("_history")
+          yield history_file
           io.class::HISTORY.clear
           previous_history.each { |line| io.class::HISTORY << line }
         end
@@ -224,7 +225,7 @@ def assert_history(expected_history, initial_irb_history, input, input_method =
         io.save_history
 
         io.load_history
-        File.open(IRB.rc_file("_history"), "r") do |f|
+        File.open(history_file, "r") do |f|
           actual_history = f.read
         end
       end
diff --git a/test/irb/test_init.rb b/test/irb/test_init.rb
index 036509813..16861a7a7 100644
--- a/test/irb/test_init.rb
+++ b/test/irb/test_init.rb
@@ -66,6 +66,57 @@ def test_rc_file_in_subdir
       end
     end
 
+    def test_rc_files
+      tmpdir = @tmpdir
+      Dir.chdir(tmpdir) do
+        ENV["XDG_CONFIG_HOME"] = "#{tmpdir}/xdg"
+        IRB.conf[:RC_NAME_GENERATOR] = nil
+        assert_includes IRB.rc_files, tmpdir+"/.irb#{IRB::IRBRC_EXT}"
+        assert_includes IRB.rc_files("_history"), tmpdir+"/.irb_history"
+        assert_file.not_exist?(tmpdir+"/xdg")
+        IRB.conf[:RC_NAME_GENERATOR] = nil
+        FileUtils.touch(tmpdir+"/.irb#{IRB::IRBRC_EXT}")
+        assert_includes IRB.rc_files, tmpdir+"/.irb#{IRB::IRBRC_EXT}"
+        assert_includes IRB.rc_files("_history"), tmpdir+"/.irb_history"
+        assert_file.not_exist?(tmpdir+"/xdg")
+      end
+    end
+
+    def test_rc_files_contains_multiple_files
+      tmpdir = @tmpdir
+      ENV["XDG_CONFIG_HOME"] = "#{tmpdir}/xdg"
+      ENV["IRBRC"] = "#{tmpdir}/irb"
+      xdg_config = ENV["XDG_CONFIG_HOME"]+"/irb/irb#{IRB::IRBRC_EXT}"
+
+      FileUtils.mkdir_p(xdg_config)
+      FileUtils.mkdir_p(ENV["IRBRC"])
+
+      Dir.chdir(tmpdir) do
+        IRB.conf[:RC_NAME_GENERATOR] = nil
+        assert_includes IRB.rc_files, ENV["IRBRC"]
+        assert_includes IRB.rc_files, xdg_config
+      end
+    ensure
+      ENV["IRBRC"] = nil
+      ENV["XDG_CONFIG_HOME"] = nil
+    end
+
+    def test_rc_files_in_subdir
+      tmpdir = @tmpdir
+      Dir.chdir(tmpdir) do
+        FileUtils.mkdir_p("#{tmpdir}/mydir")
+        Dir.chdir("#{tmpdir}/mydir") do
+          IRB.conf[:RC_NAME_GENERATOR] = nil
+          assert_includes IRB.rc_files, tmpdir+"/.irb#{IRB::IRBRC_EXT}"
+          assert_includes IRB.rc_files("_history"), tmpdir+"/.irb_history"
+          IRB.conf[:RC_NAME_GENERATOR] = nil
+          FileUtils.touch(tmpdir+"/.irb#{IRB::IRBRC_EXT}")
+          assert_includes IRB.rc_files, tmpdir+"/.irb#{IRB::IRBRC_EXT}"
+          assert_includes IRB.rc_files("_history"), tmpdir+"/.irb_history"
+        end
+      end
+    end
+
     def test_sigint_restore_default
       pend "This test gets stuck on Solaris for unknown reason; contribution is welcome" if RUBY_PLATFORM =~ /solaris/
       bundle_exec = ENV.key?('BUNDLE_GEMFILE') ? ['-rbundler/setup'] : []