In social species, the phenotype and fitness of an individual depend in part on the genotype of its social partners. However, how these indirect genetic effects affect genotype fitness in competitive situations is poorly understood in animal societies. We therefore studied phenotypic plasticity and fitness of two clones of the ant Cerapachys biroi in monoclonal and chimeric colonies. Here we show that, while clone B has lower fitness in isolation, surprisingly, it consistently outcompetes clone A in chimeras. The reason is that, in chimeras, clone B produces more individuals specializing in reproduction rather than cooperative tasks, behaving like a facultative social parasite. A cross-fostering experiment shows that the proportion of these individuals depends on intergenomic epistasis between larvae and nursing adults, explaining the flexible allocation strategy of clone B. Our results suggest that intergenomic epistasis can be the proximate mechanism for social parasitism in ants, revealing striking analogies between social insects and social microbes.