The central question addressed by most studies of sperm competition is: ‘what determines which male's sperm are used at fertilization?’ Empirical and theoretical studies that address this question have traditionally focused on adaptations which enhance male fertilization success while treating the female as a receptacle in which sperm competition is played out. Here we provide evidence which suggests that female genotype strongly influences the outcome of sperm competition. When the sperm of two males are in competition the proportion of offspring fathered by the second male to mate (P2) was found to be highly repeatable only if the male pair were mated to three different, but genetically similar females (full–sisters to each other; unrelated to either of the males). In contrast, if a male pair were mated to three females that were unrelated then P2 was either non–repeatable or marginally repeatable. We also show that male success in sperm competition is determined, to a large extent, by gamete and/or male–female compatibility. This conclusion is derived from the observation that P2 was repeatable among full–sisters mated to different, yet genetically similar male pairings, whilst P2 was non–repeatable among full–sisters mated to different, genetically distinct male pairings.