Sexual activity (mating) negatively affects immune function in various insect species, in both sexes. In the experiments reported in this manuscript, we tested if hosts adapted to regular pathogen challenges are less susceptible to mating-induced immune suppression, using experimentally evolved Drosophila melanogaster populations selected for increased post-infection survival when infected with a Gram-positive bacterium, Enterococcus faecalis. Mating increased the susceptibility of females to bacterial pathogens but in a pathogen-specific manner. Mating-induced increase in susceptibility was also affected by host evolutionary history, with females from selected populations exhibiting similar post-infection survival irrespective of mating status, while females from control populations became more susceptible to bacterial infections after mating. Post-infection survival of males, irrespective of their evolutionary history, was not affected by their mating status. We, therefore, conclude that hosts evolved to better survive bacterial infections are also better at resisting mating-induced increases in susceptibility to infections in Drosophila melanogaster.