Sex‐role‐reversed mating systems in which females compete for males and males may be choosy are usually associated with males investing more than females in offspring. We report that sex‐role reversal may also be caused by selfish genetic elements which distort the sex ratio towards females. Some populations of the butterflies Acraea encedon and Acraea encedana are extremely female biased because over 90% of females are infected with a Wolbachia bacterium that is maternally inherited and kills male embryos. Many females in these populations are virgins suggesting that their reproductive success may be limited by access to males. These females form lekking swarms at landmarks in which females exhibit behaviours which we interpret as functioning to solicit matings from males. The hypothesis that female A. encedon swarm in order to mate is supported by the finding that, in release‐recapture experiments, mated females tend to leave the swarm while unmated females remained. This behaviour is a sex‐role‐reversed form of a common mating system in insects in which males form lekking swarms at landmarks and compete for females. Female lekking swarms are absent from less female‐biased populations and here the butterflies are instead associated with resources in the form of the larval food plant.