diff --git a/.github/workflows/system-rubygems-bundler.yml b/.github/workflows/system-rubygems-bundler.yml
index a9cafcc5a289..e6de96a32124 100644
--- a/.github/workflows/system-rubygems-bundler.yml
+++ b/.github/workflows/system-rubygems-bundler.yml
@@ -50,6 +50,8 @@ jobs:
       - name: Run Test
         run: |
           bin/parallel_rspec
+        env:
+          RGV: system
       - name: Save system RubyGems version to ENV
         run: |
           RGV=$(ruby -e 'puts Gem::VERSION.split(".")[0..2].join(".")')
diff --git a/doc/GETTING_STARTED.md b/doc/GETTING_STARTED.md
index a290ecd56f27..2585588fee0c 100644
--- a/doc/GETTING_STARTED.md
+++ b/doc/GETTING_STARTED.md
@@ -73,14 +73,18 @@ For realworld higher level specs (also run in CI):
 
 ## Developing Bundler and RubyGems Together
 
-When developing Bundler features or bug fixes that require changes in RubyGems, you can set the `RGV` environment variable to point to the repository root so Bundler's test suite picks up those changes:
+Bundler's test suite runs against the RubyGems version selected by the `RGV` environment variable. It defaults to `.`, the RubyGems in this repository, so no setup is needed for the usual case of developing Bundler and RubyGems together:
 
-    RGV=.. bin/parallel_rspec
+    bin/parallel_rspec
 
 You can also test against specific RubyGems versions:
 
     RGV=v3.2.33 bin/parallel_rspec
 
+Or against the RubyGems copy shipped with your Ruby, as the system-rubygems-bundler CI job does:
+
+    RGV=system bin/parallel_rspec
+
 It's recommended to set this variable permanently using [direnv](https://direnv.net) for consistent development.
 
 ## Code Style and Quality
diff --git a/lib/bundler/rubygems_gem_installer.rb b/lib/bundler/rubygems_gem_installer.rb
index c6313ddf8d0e..d8c50556c531 100644
--- a/lib/bundler/rubygems_gem_installer.rb
+++ b/lib/bundler/rubygems_gem_installer.rb
@@ -94,6 +94,15 @@ def generate_plugins
       end
     end
 
+    # Reimplemented from RubyGems, since RubyGems older than 4.1 doesn't
+    # provide it
+    def remove_stale_plugins
+      return unless spec.plugins.empty?
+
+      ensure_writable_dir @plugins_dir
+      remove_plugins_for(spec, @plugins_dir)
+    end
+
     def warn_skipped_extensions
       return if spec.extensions.empty?
 
diff --git a/lib/bundler/vendored_tsort.rb b/lib/bundler/vendored_tsort.rb
index 8d8ab26ecef9..d7d680344efd 100644
--- a/lib/bundler/vendored_tsort.rb
+++ b/lib/bundler/vendored_tsort.rb
@@ -1,8 +1,21 @@
 # frozen_string_literal: true
 
-begin
-  require "rubygems/vendored_tsort"
-rescue LoadError
-  require "tsort"
-  Gem::TSort = TSort
+# The defined? guard avoids reopening Gem::TSort when an old RubyGems has
+# already loaded its own copy, e.g. through rubygems/request_set from
+# Gem.activate_bin_path in binstubs.
+#
+unless defined?(Gem::TSort)
+  begin
+    require "rubygems/vendored_tsort"
+  rescue LoadError
+    begin
+      # RubyGems 3.4 and 3.5 ship the same file under its pre-3.6 name.
+      # Requiring the real tsort here instead would activate the tsort
+      # default gem, and `bundler/setup` must not activate any gems.
+      require "rubygems/tsort"
+    rescue LoadError
+      require "tsort"
+      Gem::TSort = TSort
+    end
+  end
 end
diff --git a/spec/commands/exec_spec.rb b/spec/commands/exec_spec.rb
index d744fc616bf2..e7a294b42932 100644
--- a/spec/commands/exec_spec.rb
+++ b/spec/commands/exec_spec.rb
@@ -75,13 +75,13 @@
     skip "https://github.com/ruby/rubygems/issues/3351" if mswin?
     install_gemfile "source \"https://gem.repo1\"; gem \"myrack\""
     bundle "exec #{gem_cmd} --version"
-    expect(out).to eq(Gem::VERSION)
+    expect(out).to eq(exercised_rubygems_version.to_s)
   end
 
   it "works when exec'ing to rubygems through sh -c" do
     install_gemfile "source \"https://gem.repo1\"; gem \"myrack\""
     bundle "exec sh -c '#{gem_cmd} --version'"
-    expect(out).to eq(Gem::VERSION)
+    expect(out).to eq(exercised_rubygems_version.to_s)
   end
 
   it "works when exec'ing back to bundler to run a remote resolve" do
diff --git a/spec/commands/install_spec.rb b/spec/commands/install_spec.rb
index f8a134f23108..1e0e3a7c244b 100644
--- a/spec/commands/install_spec.rb
+++ b/spec/commands/install_spec.rb
@@ -1394,7 +1394,7 @@ def run
       expect(gem_make_out).not_to include("make -j8")
     end
 
-    it "uses 3 slots from the available pool when running the compilation of an extension" do
+    it "uses 3 slots from the available pool when running the compilation of an extension", rubygems: ">= 4.1.0.dev" do
       ENV.delete("MAKEFLAGS")
 
       install_gemfile(<<~G, env: { "BUNDLE_JOBS" => "8" })
@@ -1407,7 +1407,7 @@ def run
       expect(gem_make_out).to include("make -j3")
     end
 
-    it "consumes 3 slots from the pool when BUNDLE_JOBS isn't set" do
+    it "consumes 3 slots from the pool when BUNDLE_JOBS isn't set", rubygems: ">= 4.1.0.dev" do
       ENV.delete("MAKEFLAGS")
 
       install_gemfile(<<~G)
diff --git a/spec/install/gemfile/git_spec.rb b/spec/install/gemfile/git_spec.rb
index ee4c91a4f2b4..5fa740f4e1c6 100644
--- a/spec/install/gemfile/git_spec.rb
+++ b/spec/install/gemfile/git_spec.rb
@@ -114,9 +114,12 @@
       sha = git.ref_for("main", 11)
       spec_file = default_bundle_path("bundler/gems/foo-1.0-#{sha}/foo.gemspec")
       expect(spec_file).to exist
-      ruby_code = Gem::Specification.load(spec_file.to_s).to_ruby
+      # Serialize with the RubyGems that wrote the file, since `#to_ruby`
+      # output differs across RubyGems versions
+      ruby "print Gem::Specification.load(#{spec_file.to_s.dump}).to_ruby"
+      ruby_code = out
       file_code = File.read(spec_file)
-      expect(file_code).to eq(ruby_code)
+      expect(file_code.strip).to eq(ruby_code)
     end
 
     it "does not update the git source implicitly" do
diff --git a/spec/install/gems/resolving_spec.rb b/spec/install/gems/resolving_spec.rb
index 111d361aab9c..178f68e30bb6 100644
--- a/spec/install/gems/resolving_spec.rb
+++ b/spec/install/gems/resolving_spec.rb
@@ -726,7 +726,7 @@
         Because every version of require_rubygems depends on RubyGems > 9000
           and Gemfile depends on require_rubygems >= 0,
           RubyGems > 9000 is required.
-        So, because current RubyGems version is = #{Gem::VERSION},
+        So, because current RubyGems version is = #{exercised_rubygems_version},
           version solving has failed.
       E
       expect(err).to end_with(nice_error)
diff --git a/spec/install/global_cache_spec.rb b/spec/install/global_cache_spec.rb
index 259e8d57ba2e..5e5494dbe9d3 100644
--- a/spec/install/global_cache_spec.rb
+++ b/spec/install/global_cache_spec.rb
@@ -9,9 +9,10 @@
     let(:source2) { "http://gemserver.example.org" }
 
     def cache_base
-      # Use the unified global gem cache path if available (from RubyGems),
-      # otherwise fall back to the Bundler-specific cache location
-      if Gem.respond_to?(:global_gem_cache_path)
+      # Use the unified global gem cache path if the RubyGems under test
+      # provides it, otherwise fall back to the Bundler-specific cache
+      # location that Bundler uses on RubyGems older than 4.0
+      if exercised_rubygems_version >= Gem::Version.new("4.0.0.a")
         Pathname.new(Gem.global_gem_cache_path)
       else
         home(".bundle", "cache", "gems")
diff --git a/spec/runtime/self_management_spec.rb b/spec/runtime/self_management_spec.rb
index 176c2a312177..970a3869367f 100644
--- a/spec/runtime/self_management_spec.rb
+++ b/spec/runtime/self_management_spec.rb
@@ -171,11 +171,9 @@
       expect(out).to eq(previous_minor)
     end
 
-    it "requires the right bundler version from the config and run bundle CLI without re-exec" do
-      unless Bundler.rubygems.provides?(">= 4.1.0.dev")
-        skip "This spec can only run when Gem::BundlerVersionFinder.bundler_versions reads bundler configs"
-      end
-
+    # Can only run when Gem::BundlerVersionFinder.bundler_versions reads
+    # bundler configs
+    it "requires the right bundler version from the config and run bundle CLI without re-exec", rubygems: ">= 4.1.0.dev" do
       lockfile_bundled_with(current_version)
 
       bundle_config "version #{previous_minor}"
diff --git a/spec/support/filters.rb b/spec/support/filters.rb
index 2be25b4a78a6..67a32354d081 100644
--- a/spec/support/filters.rb
+++ b/spec/support/filters.rb
@@ -23,7 +23,10 @@ def inspect
 RSpec.configure do |config|
   config.filter_run_excluding realworld: true
 
-  config.filter_run_excluding rubygems: RequirementChecker.against(Gem.rubygems_version)
+  # Version-gated specs care about the RubyGems that spec-spawned processes
+  # run, which under RGV=system is older than the one loaded in this process.
+  exercised_rubygems_version = Gem::Version.new(ENV["BUNDLER_SPEC_SYSTEM_RUBYGEMS_VERSION"] || Gem::VERSION)
+  config.filter_run_excluding rubygems: RequirementChecker.against(exercised_rubygems_version)
   config.filter_run_excluding git: RequirementChecker.against(git_version)
   config.filter_run_excluding ruby_repo: !ENV["GEM_COMMAND"].nil?
   config.filter_run_excluding no_color_tty: Gem.win_platform? || !ENV["GITHUB_ACTION"].nil?
diff --git a/spec/support/helpers.rb b/spec/support/helpers.rb
index b0d4b5008ba7..8798cca57bb5 100644
--- a/spec/support/helpers.rb
+++ b/spec/support/helpers.rb
@@ -183,9 +183,22 @@ def gembin(cmd, options = {})
       sys_exec(cmd.to_s, options)
     end
 
+    # The RubyGems version that processes spawned by specs run. Under
+    # RGV=system it's the system RubyGems, which is older than the one loaded
+    # in the current process.
+    def exercised_rubygems_version
+      @exercised_rubygems_version ||= Gem::Version.new(ENV["BUNDLER_SPEC_SYSTEM_RUBYGEMS_VERSION"] || Gem::VERSION)
+    end
+
     def sys_exec(cmd, options = {}, &block)
       env = options[:env] || {}
-      env["RUBYOPT"] = opt_add(opt_add("-r#{spec_dir}/support/switch_rubygems.rb", env["RUBYOPT"]), ENV["RUBYOPT"])
+      if ENV["RGV"] == "system"
+        # Spawned processes must boot system RubyGems untouched, so don't make
+        # them switch, and drop the load path override the harness runs with.
+        env["RUBYOPT"] = opt_add(env["RUBYOPT"] || "", opt_remove("-I#{source_lib_dir}", ENV["RUBYOPT"]))
+      else
+        env["RUBYOPT"] = opt_add(opt_add("-r#{spec_dir}/support/switch_rubygems.rb", env["RUBYOPT"]), ENV["RUBYOPT"])
+      end
       options[:env] = env
 
       sh(cmd, options, &block)
diff --git a/spec/support/switch_rubygems.rb b/spec/support/switch_rubygems.rb
index 640b9f83b7d1..0958a1e82775 100644
--- a/spec/support/switch_rubygems.rb
+++ b/spec/support/switch_rubygems.rb
@@ -2,4 +2,17 @@
 
 require_relative "rubygems_version_manager"
 ENV["RGV"] ||= "."
-RubygemsVersionManager.new(ENV["RGV"]).switch
+
+# RGV=system runs specs against system RubyGems: processes spawned by specs
+# boot it untouched (see `Spec::Helpers#sys_exec`). The test harness itself
+# still runs on the checked out RubyGems, because the repo's lib/ dir is
+# unavoidably on its load path and would get mixed into an older RubyGems.
+# The system RubyGems version is captured here, while it's still the one
+# loaded, so version-gated specs can check the version actually under test.
+source = ENV["RGV"]
+if source == "system"
+  ENV["BUNDLER_SPEC_SYSTEM_RUBYGEMS_VERSION"] ||= Gem::VERSION
+  source = "."
+end
+
+RubygemsVersionManager.new(source).switch