Polygynous males must balance their limited ejaculate resources between current copulations, with putative future ones. Working on olive flies (Bactrocera oleae), our objectives were to determine (a) how males budget sperm to consecutive copulations, (b) what costs consecutive copulations incur, and (c) how male mating history affects female fecundity, fertility, and longevity. We allowed males to copulate with virgin females on successive days and monitored the fertility and fecundity of these females, and the longevity of both sexes. We found that as males gained sexual experience, latency to mate declined significantly, while copula duration increased. The number of sperm stored by females declined according to the sexual history of her mate-as males gained experience, significantly fewer sperm cells were transferred. Mated males suffered a significant longevity cost compared to virgin ones, but this cost was not compounded by additional matings. Male sexual experience affected both female fecundity and fertility. Furthermore, mating with an experienced male incurred a longevity cost to females. We conclude that non-sperm components of the male ejaculate are responsible for reducing female fecundity, fertility, and longevity, and predict that females should prefer to mate with virgin males.