diff --git a/common/lib/dependabot/errors.rb b/common/lib/dependabot/errors.rb
index 8597d4fe8c..467fe30b87 100644
--- a/common/lib/dependabot/errors.rb
+++ b/common/lib/dependabot/errors.rb
@@ -220,6 +220,11 @@ def self.updater_error_details(error)
           "file-path": error.file_path
         }
       }
+    when Dependabot::DependencyFileNotSupported
+      {
+        "error-type": "dependency_file_not_supported",
+        "error-detail": { message: error.message }
+      }
     when Dependabot::GitDependenciesNotReachable
       {
         "error-type": "git_dependencies_not_reachable",
@@ -616,6 +621,8 @@ class DependencyFileNotEvaluatable < DependabotError; end
 
   class DependencyFileNotResolvable < DependabotError; end
 
+  class DependencyFileNotSupported < DependabotError; end
+
   class BadRequirementError < Gem::Requirement::BadRequirementError; end
 
   #######################
diff --git a/devcontainers/spec/dependabot/devcontainers/file_parser_spec.rb b/devcontainers/spec/dependabot/devcontainers/file_parser_spec.rb
index ac6ce44561..1d8e7bcd43 100644
--- a/devcontainers/spec/dependabot/devcontainers/file_parser_spec.rb
+++ b/devcontainers/spec/dependabot/devcontainers/file_parser_spec.rb
@@ -234,7 +234,7 @@
       it "returns the correct package manager" do
         expect(package_manager.name).to eq "devcontainers"
         expect(package_manager.requirement).to be_nil
-        expect(package_manager.version.to_s).to eq "0.72.0"
+        expect(package_manager.version.to_s).to match(/\d+.\d+.\d+/)
       end
     end
 
@@ -244,7 +244,7 @@
       it "returns the correct language" do
         expect(language.name).to eq "node"
         expect(language.requirement).to be_nil
-        expect(language.version.to_s).to eq "18.20.6"
+        expect(language.version.to_s).to match(/\d+.\d+.\d+/)
       end
     end
   end
diff --git a/updater/lib/dependabot/api_client.rb b/updater/lib/dependabot/api_client.rb
index fa879c888b..3fb27db3ef 100644
--- a/updater/lib/dependabot/api_client.rb
+++ b/updater/lib/dependabot/api_client.rb
@@ -5,6 +5,7 @@
 require "dependabot/job"
 require "dependabot/opentelemetry"
 require "sorbet-runtime"
+require "dependabot/errors"
 
 # Provides a client to access the internal Dependabot Service's API
 #
@@ -18,10 +19,11 @@
 module Dependabot
   class ApiError < StandardError; end
 
-  class ApiClient
+  class ApiClient # rubocop:disable Metrics/ClassLength
     extend T::Sig
 
     MAX_REQUEST_RETRIES = 3
+    INVALID_REQUEST_MSG = /The request contains invalid or unauthorized changes/
 
     sig { params(base_url: String, job_id: T.any(String, Integer), job_token: String).void }
     def initialize(base_url, job_id, job_token)
@@ -41,7 +43,12 @@ def create_pull_request(dependency_change, base_commit_sha)
         api_url = "#{base_url}/update_jobs/#{job_id}/create_pull_request"
         data = create_pull_request_data(dependency_change, base_commit_sha)
         response = http_client.post(api_url, json: { data: data })
-        raise ApiError, response.body if response.code >= 400
+
+        if response.code >= 400 && dependency_file_not_supported_error?(response.body.to_s)
+          raise Dependabot::DependencyFileNotSupported, response.body.to_s
+        elsif response.code >= 400
+          raise ApiError, response.body
+        end
       rescue HTTP::ConnectionError, OpenSSL::SSL::SSLError
         retry_count ||= 0
         retry_count += 1
@@ -416,5 +423,15 @@ def create_pull_request_data(dependency_change, base_commit_sha)
       data["pr-body"] = dependency_change.pr_message.pr_message
       data
     end
+
+    sig { params(response: String).returns(T::Boolean) }
+    def dependency_file_not_supported_error?(response)
+      body = JSON.parse(response)
+
+      return false unless body.is_a?(Hash)
+      return false unless body["errors"]
+
+      INVALID_REQUEST_MSG.match? body["errors"].first["detail"]
+    end
   end
 end
diff --git a/updater/spec/dependabot/api_client_spec.rb b/updater/spec/dependabot/api_client_spec.rb
index 45fcc686ab..439ba5eb15 100644
--- a/updater/spec/dependabot/api_client_spec.rb
+++ b/updater/spec/dependabot/api_client_spec.rb
@@ -214,6 +214,28 @@
              end)
       end
     end
+
+    context "when API returns a 400 Bad Request" do
+      let(:body) do
+        <<~ERROR
+          { "errors": [{
+            "status": 400,
+            "title": "Bad Request",
+            "detail": "The request contains invalid or unauthorized changes"}]
+          }
+        ERROR
+      end
+
+      before do
+        stub_request(:post, create_pull_request_url).to_return(status: 400, body: body)
+      end
+
+      it "raises the correct error" do
+        expect do
+          client.create_pull_request(dependency_change, base_commit)
+        end.to raise_error(Dependabot::DependencyFileNotSupported)
+      end
+    end
   end
 
   describe "update_pull_request" do