Sexual conflict over reproduction can occur between males and females. In several naturally promiscuous insect species, experimental evolution studies that have enforced monogamy found evidence for sexual conflict. Here, we subjected the naturally promiscuous, sperm-heteromorphic fruit fly Drosophila pseudoobscura to enforced monogamy, standard levels of promiscuity, and elevated opportunities for promiscuity in four replicate lines. We examined the effect of male and female selection history and the proximate effect of variation in male density on female fitness parameters. We found that male density rather than male selection history explained a greater degree of female fecundity, egg hatching success, and productivity. Additionally, females selected under elevated promiscuity had greater fecundity and hatching success than did enforced monogamy females. Selection line males do not differ in their capacity to coerce females to remate, suggesting no divergence in precopulatory manipulative ability. However, these males did vary in their ability to suppress female remating, suggesting postcopulatory manipulation. These results indicate that sexual conflict can be manifested through both the proximate effects of male density and the historical levels of sexual selection and that the sexes respond differentially to these factors and further stress the multifarious channels of sexual communication that contribute to fitness.