diff --git a/providers/standard/src/airflow/providers/standard/operators/python.py b/providers/standard/src/airflow/providers/standard/operators/python.py
index 160617c2b789b..b597ef38cc5f1 100644
--- a/providers/standard/src/airflow/providers/standard/operators/python.py
+++ b/providers/standard/src/airflow/providers/standard/operators/python.py
@@ -562,6 +562,8 @@ def _execute_python_callable_in_subprocess(self, python_path: Path):
             )
 
             env_vars = dict(os.environ) if self.inherit_env else {}
+            if fd := os.getenv("__AIRFLOW_SUPERVISOR_FD"):
+                env_vars["__AIRFLOW_SUPERVISOR_FD"] = fd
             if self.env_vars:
                 env_vars.update(self.env_vars)
 
diff --git a/providers/standard/src/airflow/providers/standard/utils/python_virtualenv.py b/providers/standard/src/airflow/providers/standard/utils/python_virtualenv.py
index ee71f33a56056..891b3e0bce3a1 100644
--- a/providers/standard/src/airflow/providers/standard/utils/python_virtualenv.py
+++ b/providers/standard/src/airflow/providers/standard/utils/python_virtualenv.py
@@ -150,7 +150,7 @@ def _execute_in_subprocess(cmd: list[str], cwd: str | None = None, env: dict[str
         stdout=subprocess.PIPE,
         stderr=subprocess.STDOUT,
         bufsize=0,
-        close_fds=True,
+        close_fds=False,
         cwd=cwd,
         env=env,
     ) as proc:
diff --git a/providers/standard/src/airflow/providers/standard/utils/python_virtualenv_script.jinja2 b/providers/standard/src/airflow/providers/standard/utils/python_virtualenv_script.jinja2
index cb4b738138f07..8cb3ace35aa93 100644
--- a/providers/standard/src/airflow/providers/standard/utils/python_virtualenv_script.jinja2
+++ b/providers/standard/src/airflow/providers/standard/utils/python_virtualenv_script.jinja2
@@ -40,6 +40,23 @@ if sys.version_info >= (3,6):
         pass
 {% endif %}
 
+try:
+    from airflow.sdk.execution_time import task_runner
+except ModuleNotFoundError:
+    pass
+else:
+  {#-
+    We are in an Airflow 3.x environment, try and set up supervisor comms so
+    virtualenv can access Vars/Conn/XCom/etc that normal tasks can
+
+    We don't use the walrus operator (`:=`) below as it is possible people can
+    be using this on pre-3.8 versions of python, and while Airflow doesn't
+    support them, it's easy to not break it not using that operator here.
+  #}
+  reinit_supervisor_comms = getattr(task_runner, "reinit_supervisor_comms", None)
+  if reinit_supervisor_comms:
+      reinit_supervisor_comms()
+
 # Script
 {{ python_callable_source }}
 
@@ -49,12 +66,10 @@ if sys.version_info >= (3,6):
 import types
 
 {{ modified_dag_module_name }}  = types.ModuleType("{{ modified_dag_module_name }}")
-
 {{ modified_dag_module_name }}.{{ python_callable }} = {{ python_callable }}
-
 sys.modules["{{modified_dag_module_name}}"] = {{modified_dag_module_name}}
 
-{% endif%}
+{%- endif -%}
 
 {% if op_args or op_kwargs %}
 with open(sys.argv[1], "rb") as file:
diff --git a/providers/standard/tests/unit/standard/operators/test_python.py b/providers/standard/tests/unit/standard/operators/test_python.py
index 7526b5128f57a..9787b85a6c607 100644
--- a/providers/standard/tests/unit/standard/operators/test_python.py
+++ b/providers/standard/tests/unit/standard/operators/test_python.py
@@ -201,6 +201,7 @@ def run_as_operator(self, fn, **kwargs):
     def run_as_task(self, fn, return_ti=False, **kwargs):
         """Create TaskInstance and run it."""
         ti = self.create_ti(fn, **kwargs)
+        assert ti.task is not None
         ti.run()
         if return_ti:
             return ti
@@ -976,15 +977,16 @@ def test_return_none(self):
         def f():
             return None
 
-        task = self.run_as_task(f)
-        assert task.execute_callable() is None
+        ti = self.run_as_task(f, return_ti=True)
+        assert ti.xcom_pull() is None
 
     def test_return_false(self):
         def f():
             return False
 
-        task = self.run_as_task(f)
-        assert task.execute_callable() is False
+        ti = self.run_as_task(f, return_ti=True)
+
+        assert ti.xcom_pull() is False
 
     def test_lambda(self):
         with pytest.raises(
@@ -1149,8 +1151,8 @@ def f():
 
             return os.environ["MY_ENV_VAR"]
 
-        task = self.run_as_task(f, env_vars={"MY_ENV_VAR": "ABCDE"})
-        assert task.execute_callable() == "ABCDE"
+        ti = self.run_as_task(f, env_vars={"MY_ENV_VAR": "ABCDE"}, return_ti=True)
+        assert ti.xcom_pull() == "ABCDE"
 
     def test_environment_variables_with_inherit_env_true(self, monkeypatch):
         monkeypatch.setenv("MY_ENV_VAR", "QWERT")
@@ -1160,8 +1162,8 @@ def f():
 
             return os.environ["MY_ENV_VAR"]
 
-        task = self.run_as_task(f, inherit_env=True)
-        assert task.execute_callable() == "QWERT"
+        ti = self.run_as_task(f, inherit_env=True, return_ti=True)
+        assert ti.xcom_pull() == "QWERT"
 
     def test_environment_variables_with_inherit_env_false(self, monkeypatch):
         monkeypatch.setenv("MY_ENV_VAR", "TYUIO")
@@ -1182,8 +1184,8 @@ def f():
 
             return os.environ["MY_ENV_VAR"]
 
-        task = self.run_as_task(f, env_vars={"MY_ENV_VAR": "EFGHI"}, inherit_env=True)
-        assert task.execute_callable() == "EFGHI"
+        ti = self.run_as_task(f, env_vars={"MY_ENV_VAR": "EFGHI"}, inherit_env=True, return_ti=True)
+        assert ti.xcom_pull() == "EFGHI"
 
 
 venv_cache_path = tempfile.mkdtemp(prefix="venv_cache_path")