diff --git a/lib/bundler/dsl.rb b/lib/bundler/dsl.rb
index 000afebbbc..aad8759652 100644
--- a/lib/bundler/dsl.rb
+++ b/lib/bundler/dsl.rb
@@ -45,11 +45,15 @@ module Bundler
       with_gemfile(gemfile) do |current_gemfile|
         contents ||= Bundler.read_file(current_gemfile)
         instance_eval(contents, current_gemfile, 1)
-      rescue StandardError, ScriptError => e
-        message = "There was an error " \
-          "#{e.is_a?(GemfileEvalError) ? "evaluating" : "parsing"} " \
-          "`#{File.basename current_gemfile}`: #{e.message}"
-
+      rescue GemfileEvalError => e
+        message = "There was an error evaluating `#{File.basename current_gemfile}`: #{e.message}"
+        raise DSLError.new(message, current_gemfile, e.backtrace, contents)
+      rescue GemfileError, InvalidArgumentError, InvalidOption, DeprecatedError, ScriptError => e
+        message = "There was an error parsing `#{File.basename current_gemfile}`: #{e.message}"
+        raise DSLError.new(message, current_gemfile, e.backtrace, contents)
+      rescue StandardError => e
+        raise unless e.backtrace_locations.first.path == current_gemfile
+        message = "There was an error parsing `#{File.basename current_gemfile}`: #{e.message}"
         raise DSLError.new(message, current_gemfile, e.backtrace, contents)
       end
     end
@@ -215,7 +219,7 @@ module Bundler
     end
 
     def github(repo, options = {})
-      raise ArgumentError, "GitHub sources require a block" unless block_given?
+      raise InvalidArgumentError, "GitHub sources require a block" unless block_given?
       github_uri  = @git_sources["github"].call(repo)
       git_options = normalize_hash(options).merge("uri" => github_uri)
       git_source  = @sources.add_git_source(git_options)
diff --git a/lib/bundler/errors.rb b/lib/bundler/errors.rb
index 35b5a55038..a0ce739ad7 100644
--- a/lib/bundler/errors.rb
+++ b/lib/bundler/errors.rb
@@ -244,4 +244,6 @@ module Bundler
 
     status_code(39)
   end
+
+  class InvalidArgumentError < BundlerError; status_code(40); end
 end
diff --git a/lib/bundler/ruby_version.rb b/lib/bundler/ruby_version.rb
index 7e9e072b83..0ed5cbc6ca 100644
--- a/lib/bundler/ruby_version.rb
+++ b/lib/bundler/ruby_version.rb
@@ -23,7 +23,13 @@ module Bundler
       #   specified must match the version.
 
       @versions = Array(versions).map do |v|
-        op, v = Gem::Requirement.parse(normalize_version(v))
+        normalized_v = normalize_version(v)
+
+        unless Gem::Requirement::PATTERN.match?(normalized_v)
+          raise InvalidArgumentError, "#{v} is not a valid requirement on the Ruby version"
+        end
+
+        op, v = Gem::Requirement.parse(normalized_v)
         op == "=" ? v.to_s : "#{op} #{v}"
       end
 
diff --git a/spec/bundler/bundler/ruby_dsl_spec.rb b/spec/bundler/bundler/ruby_dsl_spec.rb
index 384ac4b8b2..c5ebbdf4db 100644
--- a/spec/bundler/bundler/ruby_dsl_spec.rb
+++ b/spec/bundler/bundler/ruby_dsl_spec.rb
@@ -80,7 +80,7 @@ RSpec.describe Bundler::RubyDsl do
     context "with two requirements in the same string" do
       let(:ruby_version) { ">= 2.0.0, < 3.0" }
       it "raises an error" do
-        expect { subject }.to raise_error(ArgumentError)
+        expect { subject }.to raise_error(Bundler::InvalidArgumentError)
       end
     end
 
@@ -168,7 +168,7 @@ RSpec.describe Bundler::RubyDsl do
         let(:file_content) { "ruby-#{version}@gemset\n" }
 
         it "raises an error" do
-          expect { subject }.to raise_error(Gem::Requirement::BadRequirementError, "Illformed requirement [\"#{version}@gemset\"]")
+          expect { subject }.to raise_error(Bundler::InvalidArgumentError, "2.0.0@gemset is not a valid requirement on the Ruby version")
         end
       end
 
diff --git a/spec/bundler/install/gemfile_spec.rb b/spec/bundler/install/gemfile_spec.rb
index 0539733d5d..96ed174e9b 100644
--- a/spec/bundler/install/gemfile_spec.rb
+++ b/spec/bundler/install/gemfile_spec.rb
@@ -66,6 +66,31 @@ RSpec.describe "bundle install" do
     end
   end
 
+  context "when an internal error happens" do
+    let(:bundler_bug) do
+      create_file("bundler_bug.rb", <<~RUBY)
+        require "bundler"
+
+        module Bundler
+          class Dsl
+            def source(source, *args, &blk)
+              nil.name
+            end
+          end
+        end
+      RUBY
+
+      bundled_app("bundler_bug.rb").to_s
+    end
+
+    it "shows culprit file and line" do
+      skip "ruby-core test setup has always \"lib\" in $LOAD_PATH so `require \"bundler\"` always activates the local version rather than using RubyGems gem activation stuff, causing conflicts" if ruby_core?
+
+      install_gemfile "source 'https://gem.repo1'", requires: [bundler_bug], artifice: nil, raise_on_error: false
+      expect(err).to include("bundler_bug.rb:6")
+    end
+  end
+
   context "with engine specified in symbol", :jruby_only do
     it "does not raise any error parsing Gemfile" do
       install_gemfile <<-G