Research on fruit fly courtship has mostly focused on males’ behavioral repertoire whereas females have been assumed to respond by either rejecting or accepting males. In many fruit fly species including Drosophila melanogaster, however, mating typically follows an extended period of courtship, which provides ample opportunities for females to inform males about their likelihood of mating. Our experiments indeed revealed that sexually immature females in both D. melanogasterand D. simulans showed responses to conspecific males that were distinct from those of sexually mature females. Furthermore, females’ responses to conspecific males were different from their responses to heterospecific males. Our data indicate that females’ behavioral repertoire early in courtship can inform males about their probability of mating if they persist in courting. We hypothesize (i) that males can rely on behavioral feedback from females for optimally allocating their courtship efforts towards distinct female classes, (ii) that males may learn to modulate their courtship behavior based on specific feedback from females, and (iii) that females may learn to alter their behavior towards distinct types of males in order to elicit the desired male response. Overall, we suggest that, although little explored, female behavior determines the dynamics of courtship and mating and can thus influence sexual selection and incipient speciation.