diff --git a/changelogs/fragments/templating-filter-generators.yml b/changelogs/fragments/templating-filter-generators.yml
new file mode 100644
index 00000000000..e0fcfe9116c
--- /dev/null
+++ b/changelogs/fragments/templating-filter-generators.yml
@@ -0,0 +1,3 @@
+bugfixes:
+  - templating - Ensure filter plugin result processing occurs under the correct call context.
+    (https://github.com/ansible/ansible/issues/85585)
diff --git a/lib/ansible/_internal/_templating/_jinja_plugins.py b/lib/ansible/_internal/_templating/_jinja_plugins.py
index 482dabfbb01..c1c5df0d87c 100644
--- a/lib/ansible/_internal/_templating/_jinja_plugins.py
+++ b/lib/ansible/_internal/_templating/_jinja_plugins.py
@@ -115,7 +115,13 @@ class JinjaPluginIntercept(c.MutableMapping):
 
         try:
             with JinjaCallContext(accept_lazy_markers=instance.accept_lazy_markers):
-                return instance.j2_function(*lazify_container_args(args), **lazify_container_kwargs(kwargs))
+                result = instance.j2_function(*lazify_container_args(args), **lazify_container_kwargs(kwargs))
+
+                if instance.plugin_type == 'filter':
+                    # ensure list conversion occurs under the call context
+                    result = _wrap_plugin_output(result)
+
+                return result
         except MarkerError as ex:
             return ex.source
         except Exception as ex:
@@ -156,7 +162,6 @@ class JinjaPluginIntercept(c.MutableMapping):
         @functools.wraps(instance.j2_function)
         def wrapper(*args, **kwargs) -> t.Any:
             result = self._invoke_plugin(instance, *args, **kwargs)
-            result = _wrap_plugin_output(result)
 
             return result
 
diff --git a/test/units/_internal/templating/test_templar.py b/test/units/_internal/templating/test_templar.py
index ed1c5eb40bb..c062d3f6b53 100644
--- a/test/units/_internal/templating/test_templar.py
+++ b/test/units/_internal/templating/test_templar.py
@@ -1078,3 +1078,18 @@ def test_marker_from_test_plugin() -> None:
     """Verify test plugins can raise MarkerError to return a Marker, and that no warnings or deprecations are emitted."""
     with emits_warnings(deprecation_pattern=[], warning_pattern=[]):
         assert TemplateEngine(variables=dict(something=TRUST.tag("{{ nope }}"))).template(TRUST.tag("{{ (something is eq {}) is undefined }}"))
+
+
+def test_filter_generator() -> None:
+    """Verify that filters which return a generator are converted to a list while under the filter's JinjaCallContext."""
+    variables = dict(
+        foo=[
+            dict(x=1, optional_var=0),
+            dict(x=2),
+        ],
+        bar=TRUST.tag("{{ foo | selectattr('optional_var', 'defined') }}"),
+    )
+
+    te = TemplateEngine(variables=variables)
+    te.template(TRUST.tag("{{ bar }}"))
+    te.template(TRUST.tag("{{ lookup('vars', 'bar') }}"))