Studies of experimental sexual selection have tested the effect of variation in the intensity of sexual selection on male investment in reproduction, particularly sperm. However, in several species, including Drosophila pseudoobscura, no sperm response to experimental evolution has occurred. Here, we take a quantitative genetics approach to examine whether genetic constraints explain the limited evolutionary response. We quantified direct and indirect genetic variation, and genetic correlations within and between the sexes, in experimental populations of D. pseudoobscura. We found that sperm number may be limited by low heritability and evolvability whereas sperm quality (length) has moderate V(A) and CV(A) but does not evolve. Likewise, the female reproductive tract, suggested to drive the evolution of sperm, did not respond to experimental sexual selection even though there was sufficient genetic variation. The lack of genetic correlations between the sexes supports the opportunity for sexual conflict over investment in sperm by males and their storage by females. Our results suggest no absolute constraint arising from a lack of direct or indirect genetic variation or patterns of genetic covariation. These patterns show why responses to experimental evolution are hard to predict, and why research on genetic variation underlying interacting reproductive traits is needed.