diff --git a/django/db/models/expressions.py b/django/db/models/expressions.py
index 89332699d5..c1a76584f0 100644
--- a/django/db/models/expressions.py
+++ b/django/db/models/expressions.py
@@ -876,8 +876,11 @@ class When(Expression):
     conditional = False
 
     def __init__(self, condition=None, then=None, **lookups):
-        if lookups and condition is None:
-            condition, lookups = Q(**lookups), None
+        if lookups:
+            if condition is None:
+                condition, lookups = Q(**lookups), None
+            elif getattr(condition, 'conditional', False):
+                condition, lookups = Q(condition, **lookups), None
         if condition is None or not getattr(condition, 'conditional', False) or lookups:
             raise TypeError(
                 'When() supports a Q object, a boolean expression, or lookups '
diff --git a/docs/ref/models/conditional-expressions.txt b/docs/ref/models/conditional-expressions.txt
index 7616b98e0a..a1e2430ec1 100644
--- a/docs/ref/models/conditional-expressions.txt
+++ b/docs/ref/models/conditional-expressions.txt
@@ -81,6 +81,10 @@ Keep in mind that each of these values can be an expression.
         >>> When(then__exact=0, then=1)
         >>> When(Q(then=0), then=1)
 
+.. versionchanged:: 3.2
+
+    Support for using the ``condition`` argument with ``lookups`` was added.
+
 ``Case``
 --------
 
diff --git a/docs/releases/3.2.txt b/docs/releases/3.2.txt
index 7aa01dcc23..2d49299440 100644
--- a/docs/releases/3.2.txt
+++ b/docs/releases/3.2.txt
@@ -178,6 +178,9 @@ Models
   supported on PostgreSQL, allows acquiring weaker locks that don't block the
   creation of rows that reference locked rows through a foreign key.
 
+* :class:`When() <django.db.models.expressions.When>` expression now allows
+  using the ``condition`` argument with ``lookups``.
+
 Requests and Responses
 ~~~~~~~~~~~~~~~~~~~~~~
 
diff --git a/tests/expressions_case/tests.py b/tests/expressions_case/tests.py
index f85def932a..efb4ba227e 100644
--- a/tests/expressions_case/tests.py
+++ b/tests/expressions_case/tests.py
@@ -6,7 +6,7 @@ from uuid import UUID
 
 from django.core.exceptions import FieldError
 from django.db.models import (
-    BinaryField, Case, CharField, Count, DurationField, F,
+    BinaryField, BooleanField, Case, CharField, Count, DurationField, F,
     GenericIPAddressField, IntegerField, Max, Min, Q, Sum, TextField,
     TimeField, UUIDField, Value, When,
 )
@@ -312,6 +312,17 @@ class CaseExpressionTests(TestCase):
             transform=attrgetter('integer', 'integer2')
         )
 
+    def test_condition_with_lookups(self):
+        qs = CaseTestModel.objects.annotate(
+            test=Case(
+                When(Q(integer2=1), string='2', then=Value(False)),
+                When(Q(integer2=1), string='1', then=Value(True)),
+                default=Value(False),
+                output_field=BooleanField(),
+            ),
+        )
+        self.assertIs(qs.get(integer=1).test, True)
+
     def test_case_reuse(self):
         SOME_CASE = Case(
             When(pk=0, then=Value('0')),
@@ -1350,6 +1361,8 @@ class CaseWhenTests(SimpleTestCase):
             When(condition=object())
         with self.assertRaisesMessage(TypeError, msg):
             When(condition=Value(1, output_field=IntegerField()))
+        with self.assertRaisesMessage(TypeError, msg):
+            When(Value(1, output_field=IntegerField()), string='1')
         with self.assertRaisesMessage(TypeError, msg):
             When()