Research into the evolution of giant sperm has uncovered a paradox within the foundations of sexual selection theory. Postcopulatory sexual selection on males (that is, sperm competition and cryptic female choice) can lead to decreased sperm numbers by favouring the production of larger sperm1. However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females2,3. As isogamy is approached (that is, as investment per gamete by males approaches that by females), sperm become less abundant, ova become relatively less rare, and competition between males for fertilization success is predicted to weaken. Sexual selection for longer sperm, therefore, is expected to be self limiting. Here we examine this paradox in Drosophila along the anisogamy–isogamy continuum using intraspecific experimental evolution techniques and interspecific comparative techniques. Our results confirm the big-sperm paradox by showing that the sex difference in sexual selection gradients4 decreases as sperm size increases. However, a resolution to the paradox is provided when this finding is interpreted in concert with the ‘opportunity for selection’ and the ‘opportunity for sexual selection’5,6. Furthermore, we show that most of the variation in measures of selection intensity is explained by sperm length and relative investment in sperm production.