Abstract: The arena of sexual selection expands after copulation to include the female reproductive tract when promiscuous females house ejaculates from more than one male. Male-male competition continues in the form of sperm competition, and female choice continues in the form of cryptic female choice. This study aims to contribute (1) to the understanding of the mechanisms underlying postcopulatory sexual selection and (2) to the unification of postcopulatory sexual selection theory and traditional sexual selection theory. Strong offensive and defensive sperm competitors are favored by postcopulatory sexual selection. Offensive and defensive sperm competitive ability were only found to be significantly repeatable in D. melanogaster across multiple sperm competition bouts between the same two males within the same female. Additionally, experimental evolution techniques revealed that the heritabilities of sperm offense and defense are low in genetically variable populations. These experiments highlight the complex nature of sperm precedence and the maintenance of genetic variation in ejaculate characteristics. Postcopulatory sexual selection on males can lead to decreased sperm numbers by favoring larger sperm. However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females. Sexual selection for longer sperm, therefore, is expected to be self-limiting. Competitive mating experiments confirmed this 'big-sperm paradox' in Drosophila . A resolution is provided by incorporating knowledge of postcopulatory processes into the interpretation of measures of sexual selection intensity. Males with little sperm competition risk or few mating opportunities should divert resources away from gamete production because sperm are no longer regarded as energetically cheap and effectively limitless in supply. This prediction was met in the giant-sperm producing D. bifurca. Solitary males with infrequent access to females were found to produce sperm at a rate much slower than males raised in constant association with females and other males. Understanding the adaptive significance of polyandry is a challenge. No direct fitness advantages of polyandry were found in D. melanogaster . If polyandry evolved to promote postcopulatory competition between males successful at precopulatory competition, then promiscuous females may benefit if these males disproportionately fertilize their eggs. However, no such indirect genetic benefits were revealed.