diff --git a/sky/core.py b/sky/core.py
index e9b0f5b5e77..594227d3838 100644
--- a/sky/core.py
+++ b/sky/core.py
@@ -498,6 +498,32 @@ def _start(
                 controller_autostop_config.enabled):
             idle_minutes_to_autostop = controller_autostop_config.idle_minutes
             down = controller_autostop_config.down
+    else:
+        # For non-controller clusters, restore autostop configuration from
+        # database if not explicitly provided.
+        if idle_minutes_to_autostop is None:
+            cluster_record = global_user_state.get_cluster_from_name(
+                cluster_name, include_user_info=False, summary_response=True)
+            if cluster_record is not None:
+                stored_autostop = cluster_record.get('autostop', -1)
+                stored_to_down = cluster_record.get('to_down', False)
+                # Restore autostop if it was previously set (autostop > 0)
+                if stored_autostop > 0:
+                    logger.warning(f'Restoring cluster {cluster_name!r} with '
+                                   f'autostop set to {stored_autostop} minutes'
+                                   f'. To turn off autostop, run: '
+                                   f'`sky autostop {cluster_name} --cancel`')
+                    idle_minutes_to_autostop = stored_autostop
+                    # Only restore 'down' if it was explicitly set and we're
+                    # restoring autostop
+                    if stored_to_down:
+                        down = stored_to_down
+                elif stored_autostop == 0:
+                    logger.warning(
+                        f'Autostop was previously set to 0 minutes '
+                        f'for cluster {cluster_name!r} so it will '
+                        'not be restored. To turn on autostop, run: '
+                        f'`sky autostop {cluster_name} -i <minutes>`')
 
     usage_lib.record_cluster_name_for_current_operation(cluster_name)
 
diff --git a/tests/smoke_tests/test_basic.py b/tests/smoke_tests/test_basic.py
index 16ee7d67441..ef325a87b68 100644
--- a/tests/smoke_tests/test_basic.py
+++ b/tests/smoke_tests/test_basic.py
@@ -328,6 +328,57 @@ def test_launch_fast_with_autostop(generic_cloud: str):
     smoke_tests_utils.run_one_test(test)
 
 
+# See cloud exclusion explanations in test_autostop
+@pytest.mark.no_fluidstack
+@pytest.mark.no_lambda_cloud
+@pytest.mark.no_ibm
+@pytest.mark.no_kubernetes
+@pytest.mark.no_hyperbolic
+@pytest.mark.no_shadeform
+@pytest.mark.no_seeweb
+def test_start_preserves_autostop(generic_cloud: str):
+    """Test that sky start preserves the autostop setting from the database."""
+    name = smoke_tests_utils.get_cluster_name()
+    autostop_timeout = 600 if generic_cloud == 'azure' else 250
+    test = smoke_tests_utils.Test(
+        'test_start_preserves_autostop',
+        [
+            # Launch cluster with autostop of 1 minute
+            f's=$(SKYPILOT_DEBUG=0 sky launch -y -c {name} --infra {generic_cloud} -i 1 {smoke_tests_utils.LOW_RESOURCE_ARG} tests/test_yamls/minimal.yaml) && {smoke_tests_utils.VALIDATE_LAUNCH_OUTPUT}',
+            f'sky logs {name} 1 --status',
+            f'sky status -r {name} | grep UP',
+            # Verify autostop is set
+            f'sky status | grep {name} | grep "1m"',
+
+            # Wait for cluster to be STOPPED from autostop
+            smoke_tests_utils.get_cmd_wait_until_cluster_status_contains(
+                cluster_name=name,
+                cluster_status=[sky.ClusterStatus.STOPPED],
+                timeout=autostop_timeout),
+
+            # Start the cluster without explicitly setting autostop - it should preserve the previous setting
+            f'sky start -y {name}',
+            # Wait for cluster to be UP
+            smoke_tests_utils.get_cmd_wait_until_cluster_status_contains(
+                cluster_name=name,
+                cluster_status=[sky.ClusterStatus.UP],
+                timeout=smoke_tests_utils.get_timeout(generic_cloud)),
+            # Verify autostop is still set (preserved from database)
+            f'sky status | grep {name} | grep "1m"',
+
+            # Wait for cluster to be STOPPED again from autostop (proving it was preserved)
+            smoke_tests_utils.get_cmd_wait_until_cluster_status_contains(
+                cluster_name=name,
+                cluster_status=[sky.ClusterStatus.STOPPED],
+                timeout=autostop_timeout),
+        ],
+        f'sky down -y {name}',
+        timeout=smoke_tests_utils.get_timeout(generic_cloud) +
+        2 * autostop_timeout,
+    )
+    smoke_tests_utils.run_one_test(test)
+
+
 # We override the AWS config to force the cluster to relaunch, so only run the
 # test on AWS.
 @pytest.mark.aws
diff --git a/tests/smoke_tests/test_cluster_job.py b/tests/smoke_tests/test_cluster_job.py
index 42f47ee9eea..f5ed083b789 100644
--- a/tests/smoke_tests/test_cluster_job.py
+++ b/tests/smoke_tests/test_cluster_job.py
@@ -1341,9 +1341,11 @@ def test_autostop_wait_for_jobs(generic_cloud: str):
                 cluster_status=[sky.ClusterStatus.STOPPED],
                 timeout=autostop_timeout),
 
-            # Ensure the cluster is UP and the autostop setting is reset ('-').
-            f'sky start -y {name}',
-            f'sky status | grep {name} | grep -E "UP\s+-"',
+            # Ensure the cluster is UP.
+            # Change the autostop setting to be very high so we can test
+            # resetting it.
+            f'sky start -y {name} -i 500',
+            f'sky status | grep {name} | grep "UP"',
 
             # Ensure the job succeeded.
             f'sky exec {name} tests/test_yamls/minimal.yaml',
@@ -1361,8 +1363,10 @@ def test_autostop_wait_for_jobs(generic_cloud: str):
                 timeout=autostop_timeout),
 
             # Test restarting the idleness timer via exec:
-            f'sky start -y {name}',
-            f'sky status | grep {name} | grep -E "UP\s+-"',
+            # Change the autostop setting to be very high so we can test
+            # resetting it.
+            f'sky start -y {name} -i 500',
+            f'sky status | grep {name} | grep "UP"',
             f'sky autostop -y {name} -i 1 --wait-for jobs',  # Idleness starts counting.
             'sleep 45',  # Almost reached the threshold.
             f'sky exec {name} echo hi',  # Should restart the timer.