diff --git a/app/models/environment.rb b/app/models/environment.rb
index 71f421fb55d6b3be8c29d4944e96efbab6c572bf..af9f45cd787e2279e9100493991847259542c7c8 100644
--- a/app/models/environment.rb
+++ b/app/models/environment.rb
@@ -84,6 +84,10 @@ class Environment < ApplicationRecord
     allow_nil: true,
     if: :description_html_changed?
 
+  validates :latest_configured_auto_stop_in,
+    length: { maximum: 255 },
+    allow_nil: true
+
   validates :kubernetes_namespace,
     allow_nil: true,
     length: 1..63,
@@ -527,6 +531,10 @@ def auto_stop_in=(value)
 
     parser = ::Gitlab::Ci::Build::DurationParser.new(value)
 
+    # The raw value is stored to allow the auto stop
+    # time to be recalculated without needing to fetch
+    # the original value from the CI job that set it.
+    self.latest_configured_auto_stop_in = value
     self.auto_stop_at = parser.seconds_from_now
   rescue ChronicDuration::DurationParseError => ex
     Gitlab::ErrorTracking.track_exception(ex, project_id: self.project_id, environment_id: self.id)
diff --git a/app/services/environments/recalculate_auto_stop_service.rb b/app/services/environments/recalculate_auto_stop_service.rb
index 8bcd7cac68f456c1caff0e551e924232ba3a4482..c82eb05508285d75b16f5b7fa255888596ea9097 100644
--- a/app/services/environments/recalculate_auto_stop_service.rb
+++ b/app/services/environments/recalculate_auto_stop_service.rb
@@ -13,13 +13,22 @@ def execute
       return unless can_set_auto_stop? && environment.present?
 
       auto_stop_in = deployable.expanded_auto_stop_in
-      auto_stop_in ||= last_successful_deployable&.expanded_auto_stop_in if can_reset_timer?
+      auto_stop_in ||= last_deployable_auto_stop_in if can_reset_timer?
 
       environment.update!(auto_stop_in: auto_stop_in) if auto_stop_in.present?
     end
 
     private
 
+    # TODO: We are transitioning from using the value stored on the last
+    # successful deployment job to the one stored on the environment. The
+    # fallback can be removed once the transition is complete (at this
+    # point the value will no longer exist at the old location).
+    # See https://gitlab.com/gitlab-org/gitlab/-/issues/545659.
+    def last_deployable_auto_stop_in
+      environment.latest_configured_auto_stop_in || last_successful_deployable&.expanded_auto_stop_in
+    end
+
     # Jobs that start an environment (using `action: start`) can also
     # specify a stop time, however this is handled by the deployment
     # process. Actions other than `start` do not create deployments,
diff --git a/db/migrate/20250613003344_add_latest_auto_stop_in_to_environments.rb b/db/migrate/20250613003344_add_latest_auto_stop_in_to_environments.rb
new file mode 100644
index 0000000000000000000000000000000000000000..47c48a3839ffefb98bd5fec59bff1702b776c212
--- /dev/null
+++ b/db/migrate/20250613003344_add_latest_auto_stop_in_to_environments.rb
@@ -0,0 +1,20 @@
+# frozen_string_literal: true
+
+class AddLatestAutoStopInToEnvironments < Gitlab::Database::Migration[2.3]
+  disable_ddl_transaction!
+  milestone '18.1'
+
+  def up
+    with_lock_retries do
+      add_column :environments, :latest_configured_auto_stop_in, :text, if_not_exists: true
+    end
+
+    add_text_limit :environments, :latest_configured_auto_stop_in, 255
+  end
+
+  def down
+    with_lock_retries do
+      remove_column :environments, :latest_configured_auto_stop_in
+    end
+  end
+end
diff --git a/db/schema_migrations/20250613003344 b/db/schema_migrations/20250613003344
new file mode 100644
index 0000000000000000000000000000000000000000..007e0c7a02b8d8bbcbb9a2bf516ab8bc40c8266d
--- /dev/null
+++ b/db/schema_migrations/20250613003344
@@ -0,0 +1 @@
+4f6c23fb39965b5fc4a4485003f45294b9998d396f35a100f819c246ba78ec21
\ No newline at end of file
diff --git a/db/structure.sql b/db/structure.sql
index 0d3e95a71c26f189cde12192cd8803e6b280f0ff..cc62b10bcc3eba1c9ed9fb7c526d0f473ea07a58 100644
--- a/db/structure.sql
+++ b/db/structure.sql
@@ -14224,7 +14224,9 @@ CREATE TABLE environments (
     description_html text,
     cached_markdown_version integer,
     auto_stop_setting smallint DEFAULT 0 NOT NULL,
+    latest_configured_auto_stop_in text,
     CONSTRAINT check_23b1eb18a2 CHECK ((char_length(flux_resource_path) <= 255)),
+    CONSTRAINT check_4a037337eb CHECK ((char_length(latest_configured_auto_stop_in) <= 255)),
     CONSTRAINT check_ad5e1ed5e1 CHECK ((char_length(description) <= 10000)),
     CONSTRAINT check_b5373a1804 CHECK ((char_length(kubernetes_namespace) <= 63)),
     CONSTRAINT check_d26221226f CHECK ((char_length(description_html) <= 50000))
diff --git a/spec/models/environment_spec.rb b/spec/models/environment_spec.rb
index 5e4a66ee1d436465d551a77497170dca431142d5..a685e109f80bc6e4917dffc1be12123cce07be71 100644
--- a/spec/models/environment_spec.rb
+++ b/spec/models/environment_spec.rb
@@ -43,6 +43,7 @@
   it { is_expected.to validate_length_of(:flux_resource_path).is_at_most(255) }
   it { is_expected.to validate_length_of(:description).is_at_most(10000) }
   it { is_expected.to validate_length_of(:description_html).is_at_most(50000) }
+  it { is_expected.to validate_length_of(:latest_configured_auto_stop_in).is_at_most(255) }
 
   describe 'validation' do
     it 'does not become invalid record when external_url is empty' do
@@ -1978,6 +1979,7 @@ def create_deployment_with_stop_action(status, pipeline, stop_action_name)
             if expected_result.is_a?(Integer) || expected_result.nil?
               subject
 
+              expect(environment.latest_configured_auto_stop_in).to eq(value)
               expect(environment.auto_stop_in).to eq(expected_result)
             else
               expect { subject }.to raise_error(expected_result)
diff --git a/spec/services/environments/recalculate_auto_stop_service_spec.rb b/spec/services/environments/recalculate_auto_stop_service_spec.rb
index 4443ce8a85f7fafbd64418091d3b22152836c40e..32c1ceb82990b83b797f023fadbd241786ee40a1 100644
--- a/spec/services/environments/recalculate_auto_stop_service_spec.rb
+++ b/spec/services/environments/recalculate_auto_stop_service_spec.rb
@@ -90,6 +90,24 @@
             it 'does not update the environment' do
               expect { recalculate }.not_to change { environment.reload.auto_stop_at }
             end
+
+            context 'when the latest_configured_auto_stop_in is stored on the environment' do
+              before do
+                environment.update!(latest_configured_auto_stop_in: '1 week')
+              end
+
+              if can_reset_timer
+                it 'updates the environment auto_stop_at' do
+                  expected_stop_at = be_like_time(1.week.from_now)
+
+                  expect { recalculate }.to change { environment.reload.auto_stop_at }.from(nil).to(expected_stop_at)
+                end
+              else
+                it 'does not update the environment' do
+                  expect { recalculate }.not_to change { environment.reload.auto_stop_at }
+                end
+              end
+            end
           end
         end
       end