diff --git a/airflow/operators/python.py b/airflow/operators/python.py
index c03f6b575033..bb37c98dafa8 100644
--- a/airflow/operators/python.py
+++ b/airflow/operators/python.py
@@ -364,7 +364,8 @@ class PythonVirtualenvOperator(PythonOperator):
     string_args). In addition, one can pass stuff through op_args and op_kwargs, and one
     can use a return value.
     Note that if your virtualenv runs in a different Python major version than Airflow,
-    you cannot use return values, op_args, or op_kwargs. You can use string_args though.
+    you cannot use return values, op_args, op_kwargs, or use any macros that are being provided to
+    Airflow through plugins. You can use string_args though.
 
     .. seealso::
         For more information on how to use this operator, take a look at the guide:
diff --git a/airflow/plugins_manager.py b/airflow/plugins_manager.py
index efd2c5682c39..c53329d52e77 100644
--- a/airflow/plugins_manager.py
+++ b/airflow/plugins_manager.py
@@ -401,6 +401,7 @@ def integrate_macros_plugins() -> None:
     global plugins
     global macros_modules
     # pylint: enable=global-statement
+    from airflow import macros
 
     if macros_modules is not None:
         return
@@ -423,3 +424,6 @@ def integrate_macros_plugins() -> None:
         if macros_module:
             macros_modules.append(macros_module)
             sys.modules[macros_module.__name__] = macros_module  # pylint: disable=no-member
+            # Register the newly created module on airflow.macros such that it
+            # can be accessed when rendering templates.
+            setattr(macros, plugin.name, macros_module)
diff --git a/airflow/utils/python_virtualenv_script.jinja2 b/airflow/utils/python_virtualenv_script.jinja2
index f2dd87525d80..95534e269519 100644
--- a/airflow/utils/python_virtualenv_script.jinja2
+++ b/airflow/utils/python_virtualenv_script.jinja2
@@ -20,6 +20,18 @@
 import {{ pickling_library }}
 import sys
 
+# Check whether Airflow is available in the environment.
+# If it is, we'll want to ensure that we integrate any macros that are being provided
+# by plugins prior to unpickling the task context.
+if sys.version_info.major >= 3 and sys.version_info.minor >= 6:
+    try:
+        from airflow.plugins_manager import integrate_macros_plugins
+        integrate_macros_plugins()
+    except ImportError:
+        # Airflow is not available in this environment, therefore we won't
+        # be able to integrate any plugin macros.
+        pass
+
 # Read args
 {% if op_args or op_kwargs %}
 with open(sys.argv[1], "rb") as file:
diff --git a/tests/plugins/test_plugins_manager.py b/tests/plugins/test_plugins_manager.py
index 2bd239f4331b..384ada0a17dd 100644
--- a/tests/plugins/test_plugins_manager.py
+++ b/tests/plugins/test_plugins_manager.py
@@ -15,6 +15,7 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+import importlib
 import logging
 import sys
 import unittest
@@ -217,6 +218,45 @@ def test_entrypoint_plugin_errors_dont_raise_exceptions(self, caplog):
             assert "Failed to import plugin test-entrypoint" in received_logs
             assert ("test.plugins.test_plugins_manager", "my_fake_module not found") in import_errors.items()
 
+    def test_registering_plugin_macros(self, request):
+        """
+        Tests whether macros that originate from plugins are being registered correctly.
+        """
+        from airflow import macros
+        from airflow.plugins_manager import integrate_macros_plugins
+
+        def cleanup_macros():
+            """Reloads the airflow.macros module such that the symbol table is reset after the test."""
+            # We're explicitly deleting the module from sys.modules and importing it again
+            # using import_module() as opposed to using importlib.reload() because the latter
+            # does not undo the changes to the airflow.macros module that are being caused by
+            # invoking integrate_macros_plugins()
+            del sys.modules['airflow.macros']
+            importlib.import_module('airflow.macros')
+
+        request.addfinalizer(cleanup_macros)
+
+        def custom_macro():
+            return 'foo'
+
+        class MacroPlugin(AirflowPlugin):
+            name = 'macro_plugin'
+            macros = [custom_macro]
+
+        with mock_plugin_manager(plugins=[MacroPlugin()]):
+            # Ensure the macros for the plugin have been integrated.
+            integrate_macros_plugins()
+            # Test whether the modules have been created as expected.
+            plugin_macros = importlib.import_module(f"airflow.macros.{MacroPlugin.name}")
+            for macro in MacroPlugin.macros:
+                # Verify that the macros added by the plugin are being set correctly
+                # on the plugin's macro module.
+                assert hasattr(plugin_macros, macro.__name__)
+            # Verify that the symbol table in airflow.macros has been updated with an entry for
+            # this plugin, this is necessary in order to allow the plugin's macros to be used when
+            # rendering templates.
+            assert hasattr(macros, MacroPlugin.name)
+
 
 class TestPluginsDirectorySource(unittest.TestCase):
     def test_should_return_correct_path_name(self):