Breeding opportunities are inherently limited for animals that live and breed in groups. Turnover in breeding positions can have marked effects on groups of cooperative breeders, particularly social carnivores. We generally know little about how breeding vacancies are filled in social carnivores and what factors might influence an individual's ability to successfully fill a vacancy. I used a long-term (11 years) genetic dataset from gray wolves to ask whether breeding vacancies were filled by individuals from within groups or by adoptees (i.e., adult animals immigrating into the group) from outside the group. Males were three times more likely than females to be adopted into breeding positions outside their group. Females typically inherited breeding positions within their natal groups (80%, n = 20), while males obtained breeding positions outside their group (76%, n = 17). Group size did not influence whether a breeding vacancy was filled by an adoptee or inherited by an individual from within the group. Prior to adoption, genetic relatedness was 30% higher in groups when females were adopted into breeding positions compared to when they inherited breeding positions from within groups. Thus, genetic relatedness within groups appears to play a role in whether females are adopted into groups or not. Because of their strong reliance on dispersal to secure a breeding position, male wolves appear to be the couriers of genetic diversity in populations of gray wolves. Many states in the United States have recently implemented hunting and trapping seasons for gray wolves. If dispersing male wolves are disproportionately harvested, genetic connectivity and diversity in populations may be affected.