diff --git a/updater/lib/dependabot/dependency_snapshot.rb b/updater/lib/dependabot/dependency_snapshot.rb
new file mode 100644
index 00000000000..a4862fc1c21
--- /dev/null
+++ b/updater/lib/dependabot/dependency_snapshot.rb
@@ -0,0 +1,81 @@
+# frozen_string_literal: true
+
+require "base64"
+require "dependabot/file_parsers"
+
+# This class describes the dependencies obtained from a project at a specific commit SHA
+# including both the Dependabot::DependencyFile objects at that reference as well as
+# means to parse them into a set of Dependabot::Dependency objects.
+#
+# This class is the input for a Dependabot::Updater process with Dependabot::DependencyChange
+# representing the output.
+module Dependabot
+  class DependencySnapshot
+    # TODO: Enforce non-nil values for job_definition["base64_dependency_files"]
+    #       and job_definition["base_commit_sha"]
+    #
+    # We historically tolerate nil values for both these keys from the `job_definition`
+    # but it doesn't seem like we should. Rather than introduce a behaviour change
+    # as part of the change introducing this class, let's do it as a follow-up.
+    def self.create_from_job_definition(job:, job_definition:)
+      decoded_dependency_files = job_definition.fetch("base64_dependency_files", []).map do |a|
+        file = Dependabot::DependencyFile.new(**a.transform_keys(&:to_sym))
+        file.content = Base64.decode64(file.content).force_encoding("utf-8") unless file.binary? && !file.deleted?
+        file
+      end
+
+      new(
+        job: job,
+        base_commit_sha: job_definition.fetch("base_commit_sha", nil),
+        dependency_files: decoded_dependency_files
+      )
+    end
+
+    attr_reader :base_commit_sha, :dependency_files
+
+    def initialize(job:, base_commit_sha:, dependency_files:)
+      @job = job
+      @base_commit_sha = base_commit_sha
+      @dependency_files = dependency_files
+    end
+
+    def dependencies
+      return @dependencies if defined?(@dependencies)
+
+      parse_files!
+    end
+
+    private
+
+    attr_reader :job
+
+    # TODO: Parse files during instantiation?
+    #
+    # To avoid having to re-home Dependabot::Updater#handle_parser_error,
+    # we perform the parsing lazily when the `dependencies` method is first
+    # referenced.
+    #
+    # We have some unusual behaviour where we handle a parse error by
+    # returning an empty dependency array in Dependabot::Updater#dependencies
+    # in order to 'fall through' to an error outcome elsewhere in the class.
+    #
+    # Given this uncertainity, and the need to significantly refactor tests,
+    # it makes sense to introduce this shim and then deal with the call
+    # site once we've split out the downstream behaviour in the updater.
+    #
+    def parse_files!
+      @dependencies = dependency_file_parser.parse
+    end
+
+    def dependency_file_parser
+      Dependabot::FileParsers.for_package_manager(job.package_manager).new(
+        dependency_files: dependency_files,
+        repo_contents_path: job.repo_contents_path,
+        source: job.source,
+        credentials: job.credentials,
+        reject_external_code: job.reject_external_code?,
+        options: job.experiments
+      )
+    end
+  end
+end
diff --git a/updater/lib/dependabot/service.rb b/updater/lib/dependabot/service.rb
index 32fe79bbb50..8be3f04937d 100644
--- a/updater/lib/dependabot/service.rb
+++ b/updater/lib/dependabot/service.rb
@@ -1,5 +1,6 @@
 # frozen_string_literal: true
 
+require "raven"
 require "terminal-table"
 require "dependabot/api_client"
 
@@ -42,6 +43,19 @@ def record_update_job_error(error_type:, error_details:, dependency: nil)
       client.record_update_job_error(error_type: error_type, error_details: error_details)
     end
 
+    def update_dependency_list(dependency_snapshot:)
+      dependency_payload = dependency_snapshot.dependencies.map do |dep|
+        {
+          name: dep.name,
+          version: dep.version,
+          requirements: dep.requirements
+        }
+      end
+      dependency_file_paths = dependency_snapshot.dependency_files.reject(&:support_file).map(&:path)
+
+      client.update_dependency_list(dependency_payload, dependency_file_paths)
+    end
+
     # This method wraps the Raven client as the Application error tracker
     # the service uses to notice errors.
     #
diff --git a/updater/lib/dependabot/update_files_command.rb b/updater/lib/dependabot/update_files_command.rb
index 018a1008045..3502b199361 100644
--- a/updater/lib/dependabot/update_files_command.rb
+++ b/updater/lib/dependabot/update_files_command.rb
@@ -2,19 +2,43 @@
 
 require "base64"
 require "dependabot/base_command"
+require "dependabot/dependency_snapshot"
 require "dependabot/updater"
 
 module Dependabot
   class UpdateFilesCommand < BaseCommand
     def perform_job
+      # We expect the FileFetcherCommand to have been executed beforehand to place
+      # encoded files and commit information in the environment, so let's retrieve
+      # and decode them into an object.
+
+      # TODO: Parse the dependency files when instantiated
+      #
+      # We can pull the error handling for parser exceptions up into this class to
+      # completely remove the concern from Dependabot::Updater.
+      #
+      # This should happen separately to introducing the class as a shim.
+      #
+      # See: updater/lib/dependabot/dependency_snapshot.rb:52
+      dependency_snapshot = Dependabot::DependencySnapshot.create_from_job_definition(
+        job: job,
+        job_definition: Environment.job_definition
+      )
+
+      # TODO: Pull fatal error handling handling up into this class
+      #
+      # As above, we can remove the responsibility for handling fatal/job halting
+      # errors from Dependabot::Updater entirely.
       Dependabot::Updater.new(
         service: service,
         job: job,
-        dependency_files: dependency_files,
-        base_commit_sha: base_commit_sha
+        dependency_snapshot: dependency_snapshot
       ).run
 
-      service.mark_job_as_processed(base_commit_sha)
+      # Finally, mark the job as processed. The Dependabot::Updater may have
+      # reported errors to the service, but we always consider the job as
+      # successfully processed unless it actually raises.
+      service.mark_job_as_processed(dependency_snapshot.base_commit_sha)
     end
 
     private
@@ -26,24 +50,5 @@ def job
         repo_contents_path: Environment.repo_contents_path
       )
     end
-
-    def dependency_files
-      @dependency_files ||=
-        Environment.job_definition["base64_dependency_files"].map do |a|
-          file = Dependabot::DependencyFile.new(**a.transform_keys(&:to_sym))
-          file.content = Base64.decode64(file.content).force_encoding("utf-8") unless file.binary? && !file.deleted?
-          file
-        end
-    end
-
-    def repo_contents_path
-      return nil unless job.clone?
-
-      Environment.repo_contents_path
-    end
-
-    def base_commit_sha
-      Environment.job_definition["base_commit_sha"]
-    end
   end
 end
diff --git a/updater/lib/dependabot/updater.rb b/updater/lib/dependabot/updater.rb
index 8190cd5dbd2..19e8d9d5ca9 100644
--- a/updater/lib/dependabot/updater.rb
+++ b/updater/lib/dependabot/updater.rb
@@ -1,13 +1,11 @@
 # frozen_string_literal: true
 
-require "raven"
 require "dependabot/config/ignore_condition"
 require "dependabot/config/update_config"
 require "dependabot/dependency_change"
 require "dependabot/environment"
 require "dependabot/experiments"
 require "dependabot/file_fetchers"
-require "dependabot/file_parsers"
 require "dependabot/file_updaters"
 require "dependabot/logger"
 require "dependabot/python"
@@ -55,11 +53,14 @@ def initialize(message, raven_context:)
       Octokit::Unauthorized => "octokit_unauthorized"
     }.freeze
 
-    def initialize(service:, job:, dependency_files:, base_commit_sha:)
+    # To do work, this class needs three arguments:
+    # - The Dependabot::Service to send events and outcomes to
+    # - The Dependabot::Job that describes the work to be done
+    # - The Dependabot::DependencySnapshot which encapsulates the starting state of the project
+    def initialize(service:, job:, dependency_snapshot:)
       @service = service
       @job = job
-      @dependency_files = dependency_files
-      @base_commit_sha = base_commit_sha
+      @dependency_snapshot = dependency_snapshot
       # TODO: Collect @created_pull_requests on the Job object?
       @created_pull_requests = []
     end
@@ -94,7 +95,7 @@ def run
     private
 
     attr_accessor :created_pull_requests
-    attr_reader :service, :job, :dependency_files, :base_commit_sha
+    attr_reader :service, :job, :dependency_snapshot
 
     def check_and_create_pr_with_error_handling(dependency)
       check_and_create_pull_request(dependency)
@@ -604,10 +605,10 @@ def existing_pull_request(updated_dependencies)
 
     # rubocop:disable Metrics/PerceivedComplexity
     def dependencies
-      all_deps = dependency_file_parser.parse
+      all_deps = dependency_snapshot.dependencies
 
       # Tell the backend about the current dependencies on the target branch
-      update_dependency_list(all_deps)
+      service.update_dependency_list(dependency_snapshot: dependency_snapshot)
 
       # Rebases and security updates have dependencies, version updates don't
       if job.dependencies
@@ -648,21 +649,10 @@ def dependencies
     end
     # rubocop:enable Metrics/PerceivedComplexity
 
-    def dependency_file_parser
-      Dependabot::FileParsers.for_package_manager(job.package_manager).new(
-        dependency_files: dependency_files,
-        repo_contents_path: job.repo_contents_path,
-        source: job.source,
-        credentials: job.credentials,
-        reject_external_code: job.reject_external_code?,
-        options: job.experiments
-      )
-    end
-
     def update_checker_for(dependency, raise_on_ignored:)
       Dependabot::UpdateCheckers.for_package_manager(job.package_manager).new(
         dependency: dependency,
-        dependency_files: dependency_files,
+        dependency_files: dependency_snapshot.dependency_files,
         repo_contents_path: job.repo_contents_path,
         credentials: job.credentials,
         ignored_versions: ignore_conditions_for(dependency),
@@ -676,7 +666,7 @@ def update_checker_for(dependency, raise_on_ignored:)
     def file_updater_for(dependencies)
       Dependabot::FileUpdaters.for_package_manager(job.package_manager).new(
         dependencies: dependencies,
-        dependency_files: dependency_files,
+        dependency_files: dependency_snapshot.dependency_files,
         repo_contents_path: job.repo_contents_path,
         credentials: job.credentials,
         options: job.experiments
@@ -755,7 +745,7 @@ def create_pull_request(dependencies, updated_dependency_files)
         updated_dependency_files: updated_dependency_files
       )
 
-      service.create_pull_request(dependency_change, base_commit_sha)
+      service.create_pull_request(dependency_change, dependency_snapshot.base_commit_sha)
 
       created_pull_requests << dependencies.map do |dep|
         {
@@ -776,7 +766,7 @@ def update_pull_request(dependencies, updated_dependency_files)
         updated_dependency_files: updated_dependency_files
       )
 
-      service.update_pull_request(dependency_change, base_commit_sha)
+      service.update_pull_request(dependency_change, dependency_snapshot.base_commit_sha)
     end
 
     def close_pull_request(reason:)
@@ -974,19 +964,6 @@ def handle_parser_error(error)
       )
     end
     # rubocop:enable Metrics/MethodLength
-
-    def update_dependency_list(dependencies)
-      service.update_dependency_list(
-        dependencies.map do |dep|
-          {
-            name: dep.name,
-            version: dep.version,
-            requirements: dep.requirements
-          }
-        end,
-        dependency_files.reject(&:support_file).map(&:path)
-      )
-    end
   end
 end
 # rubocop:enable Metrics/ClassLength
diff --git a/updater/spec/dependabot/service_spec.rb b/updater/spec/dependabot/service_spec.rb
index 0fba7f9285e..6765b0c71c5 100644
--- a/updater/spec/dependabot/service_spec.rb
+++ b/updater/spec/dependabot/service_spec.rb
@@ -3,6 +3,7 @@
 require "spec_helper"
 require "dependabot/api_client"
 require "dependabot/dependency_change"
+require "dependabot/dependency_snapshot"
 require "dependabot/service"
 
 RSpec.describe Dependabot::Service do
@@ -158,7 +159,6 @@
   describe "Instance methods delegated to @client" do
     {
       mark_job_as_processed: %w(mock_sha),
-      update_dependency_list: %w(mock_dependencies mock_dependency_file),
       record_package_manager_version: %w(mock_ecosystem mock_package_managers)
     }.each do |method, arguments|
       before { allow(mock_client).to receive(method) }
@@ -228,6 +228,80 @@
     end
   end
 
+  describe "#update_dependency_list" do
+    let(:dependency_snapshot) do
+      instance_double(Dependabot::DependencySnapshot,
+                      dependencies: [
+                        Dependabot::Dependency.new(
+                          name: "dummy-pkg-a",
+                          package_manager: "bundler",
+                          version: "2.0.0",
+                          requirements: [
+                            { file: "Gemfile", requirement: "~> 2.0.0", groups: [:default], source: nil }
+                          ]
+                        ),
+                        Dependabot::Dependency.new(
+                          name: "dummy-pkg-b",
+                          package_manager: "bundler",
+                          version: "1.1.0",
+                          requirements: [
+                            { file: "Gemfile", requirement: "~> 1.1.0", groups: [:default], source: nil }
+                          ]
+                        )
+                      ],
+                      dependency_files: [
+                        Dependabot::DependencyFile.new(
+                          name: "Gemfile",
+                          content: fixture("bundler/original/Gemfile"),
+                          directory: "/"
+                        ),
+                        Dependabot::DependencyFile.new(
+                          name: "Gemfile.lock",
+                          content: fixture("bundler/original/Gemfile.lock"),
+                          directory: "/"
+                        )
+                      ])
+    end
+
+    let(:expected_dependency_payload) do
+      [
+        {
+          name: "dummy-pkg-a",
+          version: "2.0.0",
+          requirements: [
+            {
+              file: "Gemfile",
+              requirement: "~> 2.0.0",
+              groups: [:default],
+              source: nil
+            }
+          ]
+        },
+        {
+          name: "dummy-pkg-b",
+          version: "1.1.0",
+          requirements: [
+            {
+              file: "Gemfile",
+              requirement: "~> 1.1.0",
+              groups: [:default],
+              source: nil
+            }
+          ]
+        }
+      ]
+    end
+    let(:expected_file_paths) do
+      ["/Gemfile", "/Gemfile.lock"]
+    end
+
+    it "extracts a payload from the DependencySnapshot and delegates to the client" do
+      expect(mock_client).to receive(:update_dependency_list).with(expected_dependency_payload, expected_file_paths)
+
+      service.update_dependency_list(dependency_snapshot: dependency_snapshot)
+    end
+  end
+
   describe "#noop?" do
     it "is true by default" do
       expect(service).to be_noop
diff --git a/updater/spec/dependabot/update_files_command_spec.rb b/updater/spec/dependabot/update_files_command_spec.rb
index 552f8cb4476..d2037a54b67 100644
--- a/updater/spec/dependabot/update_files_command_spec.rb
+++ b/updater/spec/dependabot/update_files_command_spec.rb
@@ -35,8 +35,7 @@
         with(
           service: service,
           job: an_object_having_attributes(id: job_id, repo_contents_path: nil),
-          dependency_files: anything,
-          base_commit_sha: base_commit_sha
+          dependency_snapshot: an_object_having_attributes(base_commit_sha: base_commit_sha)
         ).
         and_return(dummy_runner)
       expect(dummy_runner).to receive(:run)
@@ -59,8 +58,7 @@
           with(
             service: service,
             job: an_object_having_attributes(id: job_id, repo_contents_path: repo_contents_path),
-            dependency_files: anything,
-            base_commit_sha: base_commit_sha
+            dependency_snapshot: an_object_having_attributes(base_commit_sha: base_commit_sha)
           ).
           and_return(dummy_runner)
         expect(dummy_runner).to receive(:run)
diff --git a/updater/spec/dependabot/updater_spec.rb b/updater/spec/dependabot/updater_spec.rb
index 74e5cf3331a..40852ac2454 100644
--- a/updater/spec/dependabot/updater_spec.rb
+++ b/updater/spec/dependabot/updater_spec.rb
@@ -5,6 +5,7 @@
 require "bundler/compact_index_client/updater"
 require "dependabot/dependency"
 require "dependabot/dependency_file"
+require "dependabot/dependency_snapshot"
 require "dependabot/file_fetchers"
 require "dependabot/updater"
 require "dependabot/service"
@@ -70,36 +71,8 @@
       service = build_service
       updater = build_updater(service: service, job: job)
 
-      dependencies = [
-        {
-          name: "dummy-pkg-a",
-          version: "2.0.0",
-          requirements: [
-            {
-              file: "Gemfile",
-              requirement: "~> 2.0.0",
-              groups: [:default],
-              source: nil
-            }
-          ]
-        },
-        {
-          name: "dummy-pkg-b",
-          version: "1.1.0",
-          requirements: [
-            {
-              file: "Gemfile",
-              requirement: "~> 1.1.0",
-              groups: [:default],
-              source: nil
-            }
-          ]
-        }
-      ]
-      dependency_files = ["/Gemfile", "/Gemfile.lock"]
-
-      expect(service).
-        to receive(:update_dependency_list).with(dependencies, dependency_files)
+      expect(service).to receive(:update_dependency_list).
+        with(dependency_snapshot: an_instance_of(Dependabot::DependencySnapshot))
 
       updater.run
     end
@@ -1292,7 +1265,8 @@ def expect_update_checker_with_ignored_versions(versions)
               service = build_service
               updater = build_updater(service: service, job: job)
 
-              allow(updater).to receive(:dependency_files).
+              # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+              allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).
                 and_raise(Dependabot::DependencyFileNotParseable.new("path/to/file"))
 
               expect(service).to receive(:record_update_job_error).with(
@@ -1613,7 +1587,8 @@ def expect_update_checker_with_ignored_versions(versions)
         service = build_service
         updater = build_updater(service: service, job: job)
 
-        allow(updater).to receive(:dependency_files).and_raise(error)
+        # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+        allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
         expect(Raven).to receive(:capture_exception)
 
@@ -1630,7 +1605,8 @@ def expect_update_checker_with_ignored_versions(versions)
         service = build_service
         updater = build_updater(service: service, job: job)
 
-        allow(updater).to receive(:dependency_files).and_raise(error)
+        # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+        allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
         expect(service).
           to receive(:record_update_job_error).
@@ -1653,7 +1629,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(Raven).to_not receive(:capture_exception)
 
@@ -1670,7 +1647,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(service).
             to receive(:record_update_job_error).
@@ -1694,7 +1672,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(Raven).to_not receive(:capture_exception)
 
@@ -1711,7 +1690,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(service).
             to receive(:record_update_job_error).
@@ -1735,7 +1715,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(Raven).to_not receive(:capture_exception)
 
@@ -1752,7 +1733,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(service).
             to receive(:record_update_job_error).
@@ -1776,7 +1758,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(Raven).to_not receive(:capture_exception)
 
@@ -1793,7 +1776,8 @@ def expect_update_checker_with_ignored_versions(versions)
           service = build_service
           updater = build_updater(service: service, job: job)
 
-          allow(updater).to receive(:dependency_files).and_raise(error)
+          # TODO: Move this stub unto Dependabot::DependencySnapshot once it is better integrated
+          allow(Dependabot::FileParsers).to receive_message_chain(:for_package_manager, :new, :parse).and_raise(error)
 
           expect(service).
             to receive(:record_update_job_error).
@@ -2485,8 +2469,11 @@ def build_updater(service: build_service, job: build_job, dependency_files: defa
     Dependabot::Updater.new(
       service: service,
       job: job,
-      dependency_files: dependency_files,
-      base_commit_sha: "sha"
+      dependency_snapshot: Dependabot::DependencySnapshot.new(
+        job: job,
+        dependency_files: dependency_files,
+        base_commit_sha: "sha"
+      )
     )
   end