diff --git a/flytekit/remote/remote.py b/flytekit/remote/remote.py
index d031bc6aa0..76e8df1350 100644
--- a/flytekit/remote/remote.py
+++ b/flytekit/remote/remote.py
@@ -37,13 +37,19 @@
 
 from flytekit.clients.helpers import iterate_node_executions, iterate_task_executions
 from flytekit.clis.flyte_cli.main import _detect_default_config_file
+from flytekit.clis.sdk_in_container import serialize
 from flytekit.common import constants
 from flytekit.common.exceptions import user as user_exceptions
 from flytekit.common.translator import FlyteControlPlaneEntity, FlyteLocalEntity, get_serializable
 from flytekit.configuration import auth as auth_config
 from flytekit.configuration.internal import DOMAIN, PROJECT
 from flytekit.core.base_task import PythonTask
-from flytekit.core.context_manager import FlyteContextManager, ImageConfig, SerializationSettings, get_image_config
+from flytekit.core.context_manager import (
+    FlyteContextManager,
+    ImageConfig,
+    SerializationSettings,
+    get_image_config,
+)
 from flytekit.core.data_persistence import FileAccessProvider
 from flytekit.core.launch_plan import LaunchPlan
 from flytekit.core.type_engine import TypeEngine
@@ -130,6 +136,7 @@ def from_config(
         default_domain: typing.Optional[str] = None,
         config_file_path: typing.Optional[str] = None,
         grpc_credentials: typing.Optional[grpc.ChannelCredentials] = None,
+        venv_root: typing.Optional[str] = None,
     ) -> FlyteRemote:
         """Create a FlyteRemote object using flyte configuration variables and/or environment variable overrides.
 
@@ -153,6 +160,11 @@ def from_config(
             raw_output_prefix=raw_output_data_prefix,
         )
 
+        venv_root = venv_root or serialize._DEFAULT_FLYTEKIT_VIRTUALENV_ROOT
+        entrypoint = context_manager.EntrypointSettings(
+            path=os.path.join(venv_root, serialize._DEFAULT_FLYTEKIT_RELATIVE_ENTRYPOINT_LOC)
+        )
+
         return cls(
             flyte_admin_url=platform_config.URL.get(),
             insecure=platform_config.INSECURE.get(),
@@ -171,6 +183,7 @@ def from_config(
                 admin_common_models.RawOutputDataConfig(raw_output_data_prefix) if raw_output_data_prefix else None
             ),
             grpc_credentials=grpc_credentials,
+            entrypoint_settings=entrypoint,
         )
 
     def __init__(
@@ -187,6 +200,7 @@ def __init__(
         image_config: typing.Optional[ImageConfig] = None,
         raw_output_data_config: typing.Optional[admin_common_models.RawOutputDataConfig] = None,
         grpc_credentials: typing.Optional[grpc.ChannelCredentials] = None,
+        entrypoint_settings: typing.Optional[context_manager.EntrypointSettings] = None,
     ):
         """Initialize a FlyteRemote object.
 
@@ -201,7 +215,11 @@ def __init__(
         :param annotations: annotation config
         :param image_config: image config
         :param raw_output_data_config: location for offloaded data, e.g. in S3
-        :param grpc_credentials: gRPC channel credentials for connecting to flyte admin as returned by :func:`grpc.ssl_channel_credentials`
+        :param grpc_credentials: gRPC channel credentials for connecting to flyte admin as returned
+          by :func:`grpc.ssl_channel_credentials`
+        :param entrypoint_settings: EntrypointSettings object for use with Spark tasks. If supplied, this will be
+          used when serializing Spark tasks, which need to know the path to the flytekit entrypoint.py file,
+          inside the container.
         """
         remote_logger.warning("This feature is still in beta. Its interface and UX is subject to change.")
         if flyte_admin_url is None:
@@ -219,6 +237,8 @@ def __init__(
         self._labels = labels
         self._annotations = annotations
         self._raw_output_data_config = raw_output_data_config
+        # Not exposing this as a property for now.
+        self._entrypoint_settings = entrypoint_settings
 
         # Save the file access object locally, but also make it available for use from the context.
         FlyteContextManager.with_context(FlyteContextManager.current_context().with_file_access(file_access).build())
@@ -527,6 +547,7 @@ def _serialize(
                 self.image_config,
                 # https://github.com/flyteorg/flyte/issues/1359
                 env={internal.IMAGE.env_var: self.image_config.default_image.full},
+                entrypoint_settings=self._entrypoint_settings,
             ),
             entity=entity,
         )
diff --git a/plugins/flytekit-spark/tests/test_remote_register.py b/plugins/flytekit-spark/tests/test_remote_register.py
new file mode 100644
index 0000000000..67d0f63b1f
--- /dev/null
+++ b/plugins/flytekit-spark/tests/test_remote_register.py
@@ -0,0 +1,40 @@
+from flytekitplugins.spark import Spark
+from mock import MagicMock, patch
+
+from flytekit import task
+from flytekit.remote.remote import FlyteRemote
+
+
+@patch("flytekit.configuration.platform.URL")
+@patch("flytekit.configuration.platform.INSECURE")
+def test_spark_template_with_remote(mock_insecure, mock_url):
+    @task(task_config=Spark(spark_conf={"spark": "1"}))
+    def my_spark(a: str) -> int:
+        return 10
+
+    @task
+    def my_python_task(a: str) -> int:
+        return 10
+
+    mock_url.get.return_value = "localhost"
+
+    mock_insecure.get.return_value = True
+    mock_client = MagicMock()
+
+    remote = FlyteRemote.from_config("p1", "d1")
+
+    remote._image_config = MagicMock()
+    remote._client = mock_client
+
+    remote.register(my_spark)
+    serialized_spec = mock_client.create_task.call_args.kwargs["task_spec"]
+
+    # Check if the serialized spark task has mainApplicaitonFile field set.
+    assert serialized_spec.template.custom["mainApplicationFile"]
+    assert serialized_spec.template.custom["sparkConf"]
+
+    remote.register(my_python_task)
+    serialized_spec = mock_client.create_task.call_args.kwargs["task_spec"]
+
+    # Check if the serialized python task has no mainApplicaitonFile field set by default.
+    assert serialized_spec.template.custom is None