Women remain universally underrepresented in the top leadership positions. A comparative evolutionary framework may offer new insights into the value of and potential barriers to female leadership. Here we define leaders as individuals who impose a disproportional influence on the collective behaviors of group members. We reviewed data for 76 social species of non-human mammals to reveal the circumstances favoring female leadership and species exhibiting female-biased leadership in two or more contexts (e.g., collective movements, group foraging, conflict resolution within groups, or conflicts between groups). Although rare across the lineage, female-biased leadership is pervasive in killer whales, lions, spotted hyenas, bonobos, lemurs, and elephants; leaders emerge without coercion and followers benefit from the social support and/or ecological knowledge from elder females. Our synthesis elucidates barriers to female leadership, but also reveals that traditional operationalizations of leadership are themselves male-biased. We therefore propose a new agenda for assessing the overlooked ways that females exert influence in groups.