Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1,2,3,4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5,6,7,8,9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10,11,12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a ‘pure cooperative’ strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a ‘mixed’ strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population.