Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are key to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study we show that in honey bee (Apis mellifera) colonies the social environment of a worker, i.e. the presence and relatedness of the queens in a worker’s natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift, and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker’s subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicate that honey bee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.