Nonbreeding helpers can greatly improve the survival of young and reproductive fitness of breeders in many cooperatively breeding species. Breeder turnover, in turn, can have profound effects on dispersal decisions made by helpers. Despite its importance in explaining group size and predicting population demography of cooperative breeders, our current understanding of how individual traits influence animal behavior after disruptions to social structure is incomplete particularly for terrestrial mammals. We used 12 years of genetic sampling and group pedigrees of gray wolves (Canis lupus) in Idaho, USA, to ask questions about how breeder turnover affected the apparent decisions by mature helpers (>2-year-old) to stay or leave a group over a one-year time interval. We found that helpers showed plasticity in their responses to breeder turnover. Most notably, helpers varied by sex and appeared to base dispersal decisions on the sex of the breeder that was lost as well. Male and female helpers stayed in a group slightly more often when there was breeder turnover of the same sex, although males that stayed were often recent adoptees in the group. Males, however, appeared to remain in a group less often when there was breeding female turnover likely because such vacancies were typically filled by related females from the males’ natal group (i.e., inbreeding avoidance).  We show that helpers exploit instability in the breeding pair to secure future breeding opportunities for themselves. The confluence of breeder turnover, helper sex, and dispersal and breeding strategies merge to influence group composition in gray wolves.