Across human societies, female sexuality is suppressed by gendered double standards, slut shaming, sexist rape laws, and honour killings. The question of what motivates societies to punish promiscuous women, however, has been contested. Although some have argued that men suppress female sexuality to increase paternity certainty, others maintain that this is an example of intrasexual competition. Here we show that both sexes are averse to overt displays of female sexuality, but that motivation is sex-specific. In all studies, participants played an economic game with a female partner whose photograph either signalled that she was sexually-accessible or sexually-restricted. In study 1, we found that men and women are less altruistic in a Dictator Game (DG) when partnered with a woman signalling sexual-accessibility. Both sexes were less trusting of sexually-accessible women in a Trust Game (TG) (study 2); women (but not men), however, inflicted costly punishment on a sexually-accessible woman in an Ultimatum Game (UG) (study 3). Our results demonstrate that both sexes are averse to overt sexuality in women, whilst highlighting potential differences in motivation.