In Drosophila melanogaster, males engage in both extensive pre-and postcopulatory competition for the opportunity to mate with females and subsequently sire offspring. The selection pressure for increased male reproductive success has resulted in the evolution of a wide diversity of sexual traits. However, despite strong selection, individuals often exhibit considerable phenotypic variation in the expression of these traits, and it is unclear if any of this variation is due to underlying genetic trade-offs. Here, using hemiclonal flies, we examine how male reproductive success covaries with their ability to induce long-term stimulation of oogenesis and oviposition in their mates, and how this relationship may change over time. We found that males from hemiclone lines with phenotypes that were more successful in a short-term reproductive “scramble” environment were less effective at stimulating long-term fecundity in females. Furthermore, we observed that males from hemiclone lines that showed the most improvement over a longer reproductive interaction period also tended to stimulate higher long-term fecundity in females. Together, these results indicate the presence of genetic trade-offs between different male reproductive traits, and offer insights into the maintenance of their variation.