diff --git a/activerecord/lib/active_record/associations/collection_association.rb b/activerecord/lib/active_record/associations/collection_association.rb
index c56b118129246..9ae36ecce3444 100644
--- a/activerecord/lib/active_record/associations/collection_association.rb
+++ b/activerecord/lib/active_record/associations/collection_association.rb
@@ -276,6 +276,8 @@ def target=(record)
         return super unless reflection.klass.has_many_inversing
 
         case record
+        when nil
+          # It's not possible to remove the record from the inverse association.
         when Array
           super
         else
diff --git a/activerecord/test/cases/associations/belongs_to_associations_test.rb b/activerecord/test/cases/associations/belongs_to_associations_test.rb
index b94e93a124f8f..53a1ed654c36a 100644
--- a/activerecord/test/cases/associations/belongs_to_associations_test.rb
+++ b/activerecord/test/cases/associations/belongs_to_associations_test.rb
@@ -1205,6 +1205,20 @@ def test_reassigning_the_parent_id_updates_the_object
     assert_equal companies(:another_firm), client.firm_with_condition
   end
 
+  def test_assigning_nil_on_an_association_clears_the_associations_inverse
+    with_has_many_inversing do
+      book = Book.create!
+      citation = book.citations.create!
+
+      assert_same book, citation.book
+
+      assert_nothing_raised do
+        citation.book = nil
+        citation.save!
+      end
+    end
+  end
+
   def test_clearing_an_association_clears_the_associations_inverse
     author = Author.create(name: "Jimmy Tolkien")
     post = author.create_post(title: "The silly medallion", body: "")