SignificanceSuccessful pregnancy requires establishment of immune tolerance for invading fetal trophoblasts, as well as immunity to a variety of pathogens that cause placental and congenital infections. Decidual CD8+ T cells are key cells for recognition and response to foreign fetal, placental, and viral antigens at the maternal–fetal interface. Thus, regulation of decidual CD8+ T cell activation and cytotoxicity is crucial for a healthy pregnancy. Here, we demonstrate that decidual CD8+ T cells have a mixed profile of T cell dysfunction, activation, and effector function, which allows for both immune tolerance and immunity. This is of great relevance for understanding the development of pregnancy complications as well as prevention of congenital infections that occur as result of impaired placental immunity.