This article explores the ambivalence of the human social brain using theoretical and empirical arguments from evolutionary anthropology and psychology. The social brain has evolved through the differentiation of both emotions and the ability to mentalize. With the self-reinforcing cultural dynamics, markers of trust and group affiliation became important for cooperation during evolution. The result is a coalitional psychology that explains cooperation within the group, but in conjunction with dehumanization, also the rejection of foreign groups. The ambivalence of the social brain thus lies in the fact that prosociality within the in-group resulted from the same evolutionary mechanism as the ethnic-cultural boundary drawing between groups, namely cultural group selection as a component of multilevel selection.