diff --git a/silent/tests/testdata/err-glob-not-found.txt b/silent/tests/testdata/err-glob-not-found.txt
new file mode 100644
index 00000000000..3df45959567
--- /dev/null
+++ b/silent/tests/testdata/err-glob-not-found.txt
@@ -0,0 +1,15 @@
+! dependabot update -f input.yml --local . --updater-image ghcr.io/dependabot/dependabot-updater-silent
+stderr dependency_file_not_found
+
+# Testing glob configuration when there are no manifests.
+
+-- input.yml --
+job:
+  package-manager: "silent"
+  source:
+    directories:
+      - "**/*"
+    provider: example
+    hostname: example.com
+    api-endpoint: https://example.com/api/v3
+    repo: dependabot/smoke-tests
diff --git a/silent/tests/testdata/vu-group-multidir-all.txt b/silent/tests/testdata/vu-group-multidir-all.txt
index ddb277c011b..3efe2661c99 100644
--- a/silent/tests/testdata/vu-group-multidir-all.txt
+++ b/silent/tests/testdata/vu-group-multidir-all.txt
@@ -120,5 +120,3 @@ job:
         - dependency-name: dependency-c
           dependency-version: 3.2.5
           directory: "/bar"
-  experiments:
-    dependency_has_directory: true
diff --git a/silent/tests/testdata/vu-group-multidir-semver.txt b/silent/tests/testdata/vu-group-multidir-semver.txt
index 6d9d1d795f3..49ee1c14d6a 100644
--- a/silent/tests/testdata/vu-group-multidir-semver.txt
+++ b/silent/tests/testdata/vu-group-multidir-semver.txt
@@ -3,7 +3,7 @@
 dependabot update -f input.yml --local . --updater-image ghcr.io/dependabot/dependabot-updater-silent
 stdout -count=2 create_pull_request
 pr-created foo/expected-1.json bar/expected-1.json
-pr-created foo/expected-2.json
+pr-created foo/expected-2.json bar/expected-2.json
 
 # When there is the same dependency in both directories, one is a major update the other a patch,
 # and the user asked for majors in one group and minors in the other, we should create two group PRs
@@ -32,6 +32,12 @@ pr-created foo/expected-2.json
   "dependency-b": { "version": "2.0.1" }
 }
 
+-- bar/expected-2.json --
+{
+  "dependency-a": { "version": "2.0.1" },
+  "dependency-b": { "version": "1.0.0" }
+}
+
 -- foo/expected-2.json --
 {
   "dependency-a": { "version": "1.0.0" },
@@ -77,5 +83,3 @@ job:
         update-types:
           - minor
           - patch
-  experiments:
-    dependency_has_directory: true
diff --git a/updater/lib/dependabot/dependency_snapshot.rb b/updater/lib/dependabot/dependency_snapshot.rb
index 108a3fd4e88..9fe29693748 100644
--- a/updater/lib/dependabot/dependency_snapshot.rb
+++ b/updater/lib/dependabot/dependency_snapshot.rb
@@ -55,11 +55,13 @@ def all_dependencies
 
     sig { returns(T::Array[Dependabot::DependencyFile]) }
     def dependency_files
+      assert_current_directory_set!
       @dependency_files.select { |f| f.directory == @current_directory }
     end
 
     sig { returns(T::Array[Dependabot::Dependency]) }
     def dependencies
+      assert_current_directory_set!
       T.must(@dependencies[@current_directory])
     end
 
@@ -103,10 +105,22 @@ def job_group
       @dependency_group_engine.find_group(name: T.must(job.dependency_group_to_refresh))
     end
 
+    sig { params(group: Dependabot::DependencyGroup).void }
+    def mark_group_handled(group)
+      directories.each do |directory|
+        @current_directory = directory
+
+        # add the existing dependencies in the group so individual updates don't try to update them
+        add_handled_dependencies(dependencies_in_existing_pr_for_group(group).filter_map { |d| d["dependency-name"] })
+        # also add dependencies that might be in the group, as a rebase would add them;
+        # this avoids individual PR creation that immediately is superseded by a group PR supersede
+        add_handled_dependencies(group.dependencies.map(&:name))
+      end
+    end
+
     sig { params(dependency_names: T.any(String, T::Array[String])).void }
     def add_handled_dependencies(dependency_names)
-      raise "Current directory not set" if @current_directory == ""
-
+      assert_current_directory_set!
       set = @handled_dependencies[@current_directory] || Set.new
       set += Array(dependency_names)
       @handled_dependencies[@current_directory] = set
@@ -114,18 +128,10 @@ def add_handled_dependencies(dependency_names)
 
     sig { returns(T::Set[String]) }
     def handled_dependencies
-      raise "Current directory not set" if @current_directory == ""
-
+      assert_current_directory_set!
       T.must(@handled_dependencies[@current_directory])
     end
 
-    # rubocop:disable Performance/Sum
-    sig { returns(T::Set[String]) }
-    def handled_dependencies_all_directories
-      T.must(@handled_dependencies.values.reduce(&:+))
-    end
-    # rubocop:enable Performance/Sum
-
     sig { params(dir: String).void }
     def current_directory=(dir)
       @current_directory = dir
@@ -142,10 +148,6 @@ def ungrouped_dependencies
       # If no groups are defined, all dependencies are ungrouped by default.
       return allowed_dependencies unless groups.any?
 
-      if Dependabot::Experiments.enabled?(:dependency_has_directory)
-        return allowed_dependencies.reject { |dep| handled_dependencies_all_directories.include?(dep.name) }
-      end
-
       # Otherwise return dependencies that haven't been handled during the group update portion.
       allowed_dependencies.reject { |dep| handled_dependencies.include?(dep.name) }
     end
@@ -184,6 +186,8 @@ def initialize(job:, base_commit_sha:, dependency_files:) # rubocop:disable Metr
       end
 
       job.source.directory = @original_directory
+      # reset to ensure we don't accidentally use it later without setting it
+      @current_directory = ""
       return unless job.source.directory
 
       @current_directory = T.must(job.source.directory)
@@ -210,6 +214,7 @@ def parse_files!
 
     sig { returns(Dependabot::FileParsers::Base) }
     def dependency_file_parser
+      assert_current_directory_set!
       job.source.directory = @current_directory
       Dependabot::FileParsers.for_package_manager(job.package_manager).new(
         dependency_files: dependency_files,
@@ -220,5 +225,22 @@ def dependency_file_parser
         options: job.experiments
       )
     end
+
+    sig { params(group: Dependabot::DependencyGroup).returns(T::Array[T::Hash[String, String]]) }
+    def dependencies_in_existing_pr_for_group(group)
+      job.existing_group_pull_requests.find do |pr|
+        pr["dependency-group-name"] == group.name
+      end&.fetch("dependencies", []) || []
+    end
+
+    sig { void }
+    def assert_current_directory_set!
+      if @current_directory == "" && directories.count == 1
+        @current_directory = T.must(directories.first)
+        return
+      end
+
+      raise DependabotError, "Assertion failed: Current directory not set" if @current_directory == ""
+    end
   end
 end
diff --git a/updater/lib/dependabot/file_fetcher_command.rb b/updater/lib/dependabot/file_fetcher_command.rb
index e18898ea494..927db8f3e55 100644
--- a/updater/lib/dependabot/file_fetcher_command.rb
+++ b/updater/lib/dependabot/file_fetcher_command.rb
@@ -99,6 +99,7 @@ def file_fetcher_for_directory(directory)
       @file_fetchers[directory] ||= create_file_fetcher(directory: directory)
     end
 
+    # rubocop:disable Metrics/PerceivedComplexity
     def dependency_files_for_multi_directories
       return @dependency_files_for_multi_directories if defined?(@dependency_files_for_multi_directories)
 
@@ -128,7 +129,14 @@ def dependency_files_for_multi_directories
         post_ecosystem_versions(ff) if should_record_ecosystem_versions?
         files
       end.compact
+
+      if @dependency_files_for_multi_directories.empty?
+        raise Dependabot::DependencyFileNotFound, job.source.directories.join(", ")
+      end
+
+      @dependency_files_for_multi_directories
     end
+    # rubocop:enable Metrics/PerceivedComplexity
 
     def dependency_files
       return @dependency_files if defined?(@dependency_files)
diff --git a/updater/lib/dependabot/updater/group_update_creation.rb b/updater/lib/dependabot/updater/group_update_creation.rb
index ba975dc5c0d..50d5ddca9d6 100644
--- a/updater/lib/dependabot/updater/group_update_creation.rb
+++ b/updater/lib/dependabot/updater/group_update_creation.rb
@@ -54,8 +54,7 @@ def compile_all_dependency_changes_for(group)
 
         Dependabot.logger.info("Updating the #{job.source.directory} directory.")
         group.dependencies.each do |dependency|
-          # We check dependency_snapshot.handled_dependencies instead of handled_dependencies_all_directories here
-          # because we still want to update a dependency if it's been updated in another manifest files,
+          # We still want to update a dependency if it's been updated in another manifest files,
           # but we should skip it if it's been updated in _the same_ manifest file
           if dependency_snapshot.handled_dependencies.include?(dependency.name)
             Dependabot.logger.info(
@@ -427,13 +426,6 @@ def pr_exists_for_dependency_group?(group)
         job.existing_group_pull_requests.any? { |pr| pr["dependency-group-name"] == group.name }
       end
 
-      sig { params(group: Dependabot::DependencyGroup).returns(T::Array[T::Hash[String, String]]) }
-      def dependencies_in_existing_pr_for_group(group)
-        job.existing_group_pull_requests.find do |pr|
-          pr["dependency-group-name"] == group.name
-        end&.fetch("dependencies", [])
-      end
-
       sig do
         params(
           dependency: T.nilable(Dependabot::Dependency),
diff --git a/updater/lib/dependabot/updater/operations/group_update_all_versions.rb b/updater/lib/dependabot/updater/operations/group_update_all_versions.rb
index 06a365bf78e..afb90751448 100644
--- a/updater/lib/dependabot/updater/operations/group_update_all_versions.rb
+++ b/updater/lib/dependabot/updater/operations/group_update_all_versions.rb
@@ -99,7 +99,6 @@ def perform
         sig { returns(Dependabot::Updater::ErrorHandler) }
         attr_reader :error_handler
 
-        # rubocop:disable Metrics/AbcSize
         sig { returns(T::Array[Dependabot::DependencyGroup]) }
         def run_grouped_dependency_updates
           Dependabot.logger.info("Starting grouped update job for #{job.source.repo}")
@@ -113,14 +112,7 @@ def run_grouped_dependency_updates
               Dependabot.logger.info(
                 "Deferring creation of a new pull request. The existing pull request will update in a separate job."
               )
-
-              # add the dependencies in the group so individual updates don't try to update them
-              dependency_snapshot.add_handled_dependencies(
-                dependencies_in_existing_pr_for_group(group).filter_map { |d| d["dependency-name"] }
-              )
-              # also add dependencies that might be in the group, as a rebase would add them;
-              # this avoids individual PR creation that immediately is superseded by a group PR supersede
-              dependency_snapshot.add_handled_dependencies(group.dependencies.map(&:name))
+              dependency_snapshot.mark_group_handled(group)
               next
             end
 
@@ -128,17 +120,11 @@ def run_grouped_dependency_updates
           end
 
           groups_without_pr.each do |group|
-            grouped_update_result = run_grouped_update_for(group)
-            if grouped_update_result
-              # Add the actual updated dependencies to the handled list so they don't get updated individually.
-              dependency_snapshot.add_handled_dependencies(grouped_update_result.updated_dependencies.map(&:name))
-            else
-              # The update failed, add the suspected dependencies to the handled list so they don't update individually.
-              dependency_snapshot.add_handled_dependencies(group.dependencies.map(&:name))
-            end
+            dependency_change = run_grouped_update_for(group)
+            # The update failed, add the suspected dependencies to the handled list so they don't update individually.
+            dependency_snapshot.mark_group_handled(group) if dependency_change.nil?
           end
         end
-        # rubocop:enable Metrics/AbcSize
 
         sig { params(group: Dependabot::DependencyGroup).returns(T.nilable(Dependabot::DependencyChange)) }
         def run_grouped_update_for(group)
diff --git a/updater/lib/dependabot/updater/operations/refresh_group_update_pull_request.rb b/updater/lib/dependabot/updater/operations/refresh_group_update_pull_request.rb
index f535f92d934..4f813232748 100644
--- a/updater/lib/dependabot/updater/operations/refresh_group_update_pull_request.rb
+++ b/updater/lib/dependabot/updater/operations/refresh_group_update_pull_request.rb
@@ -108,9 +108,7 @@ def perform # rubocop:disable Metrics/AbcSize
             dependency_snapshot.groups.each do |group|
               next unless group.name != job_group.name && pr_exists_for_dependency_group?(group)
 
-              dependency_snapshot.add_handled_dependencies(
-                dependencies_in_existing_pr_for_group(group).filter_map { |d| d["dependency-name"] }
-              )
+              dependency_snapshot.mark_group_handled(group)
             end
 
             if dependency_change.nil?
diff --git a/updater/spec/dependabot/dependency_snapshot_spec.rb b/updater/spec/dependabot/dependency_snapshot_spec.rb
index 876337f48e1..2830dfe8fc4 100644
--- a/updater/spec/dependabot/dependency_snapshot_spec.rb
+++ b/updater/spec/dependabot/dependency_snapshot_spec.rb
@@ -140,59 +140,6 @@
     end
   end
 
-  describe "::handled_dependencies_all_directories" do
-    subject(:create_dependency_snapshot) do
-      described_class.create_from_job_definition(
-        job: job,
-        job_definition: job_definition
-      )
-    end
-
-    let(:job_definition) do
-      {
-        "base_commit_sha" => base_commit_sha,
-        "base64_dependency_files" => encode_dependency_files(dependency_files)
-      }
-    end
-
-    it "handles dependencies" do
-      snapshot = create_dependency_snapshot
-      snapshot.add_handled_dependencies(%w(a b))
-      expect(snapshot.handled_dependencies_all_directories).to eq(Set.new(%w(a b)))
-    end
-
-    context "when there are multiple directories" do
-      let(:directory) { nil }
-      let(:directories) { %w(/foo /bar) }
-      let(:dependency_files) do
-        [
-          Dependabot::DependencyFile.new(
-            name: "Gemfile",
-            content: fixture("bundler/original/Gemfile"),
-            directory: "/foo"
-          ),
-          Dependabot::DependencyFile.new(
-            name: "Gemfile",
-            content: fixture("bundler/original/Gemfile"),
-            directory: "/bar"
-          )
-        ]
-      end
-
-      it "is agnostic of the current directory" do
-        snapshot = create_dependency_snapshot
-        snapshot.current_directory = "/foo"
-        snapshot.add_handled_dependencies("a")
-        snapshot.current_directory = "/bar"
-        snapshot.add_handled_dependencies("b")
-
-        expect(snapshot.handled_dependencies_all_directories).to eq(Set.new(%w(a b)))
-        snapshot.current_directory = "/bar"
-        expect(snapshot.handled_dependencies_all_directories).to eq(Set.new(%w(a b)))
-      end
-    end
-  end
-
   describe "::create_from_job_definition" do
     subject(:create_dependency_snapshot) do
       described_class.create_from_job_definition(
@@ -330,4 +277,119 @@
       end
     end
   end
+
+  describe "::mark_group_handled" do
+    subject(:create_dependency_snapshot) do
+      described_class.create_from_job_definition(
+        job: job,
+        job_definition: job_definition
+      )
+    end
+
+    let(:job) do
+      instance_double(Dependabot::Job,
+                      package_manager: "bundler",
+                      security_updates_only?: false,
+                      repo_contents_path: nil,
+                      credentials: [],
+                      reject_external_code?: false,
+                      source: source,
+                      dependency_groups: dependency_groups,
+                      allowed_update?: true,
+                      dependency_group_to_refresh: nil,
+                      dependencies: nil,
+                      experiments: { large_hadron_collider: true },
+                      existing_group_pull_requests: existing_group_pull_requests)
+    end
+
+    let(:source) do
+      Dependabot::Source.new(
+        provider: "github",
+        repo: "dependabot-fixtures/dependabot-test-ruby-package",
+        directories: %w(/foo /bar),
+        branch: nil,
+        api_endpoint: "https://api.github.com/",
+        hostname: "github.com"
+      )
+    end
+
+    let(:dependency_groups) do
+      [
+        {
+          "name" => "group-a",
+          "rules" => {
+            "patterns" => ["dummy-pkg-*"],
+            "exclude-patterns" => ["dummy-pkg-b"]
+          }
+        }
+      ]
+    end
+
+    let(:existing_group_pull_requests) do
+      [
+        {
+          "group" => "group-a",
+          "dependencies" => %w(dummy-pkg-a)
+        }
+      ]
+    end
+
+    let(:job_definition) do
+      {
+        "base_commit_sha" => base_commit_sha,
+        "base64_dependency_files" => encode_dependency_files(dependency_files)
+      }
+    end
+
+    let(:dependency_files) do
+      [
+        Dependabot::DependencyFile.new(
+          name: "Gemfile",
+          content: fixture("bundler/original/Gemfile"),
+          directory: "/foo"
+        ),
+        Dependabot::DependencyFile.new(
+          name: "Gemfile.lock",
+          content: fixture("bundler/original/Gemfile.lock"),
+          directory: "/foo"
+        ),
+        Dependabot::DependencyFile.new(
+          name: "Gemfile",
+          content: fixture("bundler/original/Gemfile"),
+          directory: "/bar"
+        ),
+        Dependabot::DependencyFile.new(
+          name: "Gemfile.lock",
+          content: fixture("bundler/original/Gemfile.lock"),
+          directory: "/bar"
+        )
+      ]
+    end
+
+    it "marks the dependencies handled for all directories" do
+      snapshot = create_dependency_snapshot
+      snapshot.mark_group_handled(snapshot.groups.first)
+
+      snapshot.current_directory = "/foo"
+      expect(snapshot.handled_dependencies).to eq(Set.new(%w(dummy-pkg-a)))
+
+      snapshot.current_directory = "/bar"
+      expect(snapshot.handled_dependencies).to eq(Set.new(%w(dummy-pkg-a)))
+    end
+
+    context "when there are no existing group pull requests" do
+      let(:existing_group_pull_requests) { [] }
+
+      it "marks the dependencies that would have been covered as handled" do
+        snapshot = create_dependency_snapshot
+        snapshot.mark_group_handled(snapshot.groups.first)
+
+        snapshot.current_directory = "/foo"
+        expect(snapshot.handled_dependencies).to eq(Set.new(%w(dummy-pkg-a)))
+
+        snapshot.current_directory = "/bar"
+        expect(snapshot.handled_dependencies).to eq(Set.new(%w(dummy-pkg-a)))
+      end
+    end
+  end
 end
diff --git a/updater/spec/dependabot/updater/operations/refresh_group_update_pull_request_spec.rb b/updater/spec/dependabot/updater/operations/refresh_group_update_pull_request_spec.rb
index ceb22fe739b..3825770be6d 100644
--- a/updater/spec/dependabot/updater/operations/refresh_group_update_pull_request_spec.rb
+++ b/updater/spec/dependabot/updater/operations/refresh_group_update_pull_request_spec.rb
@@ -70,11 +70,6 @@
 
     before do
       stub_rubygems_calls
-      Dependabot::Experiments.register("dependency_has_directory", true)
-    end
-
-    after do
-      Dependabot::Experiments.reset!
     end
 
     it "updates the existing pull request without errors" do