Adaptations conferring resistance to xenobiotics (antibiotics, insecticides, herbicides, etc.) are often costly to the organism's fitness in the absence of the selecting agent. In such conditions, and unless other mutations compensate for the costs of resistance, sensitive individuals are expected to out‐reproduce resistant individuals and drive resistance alleles to a low frequency, with the rate and magnitude of this decline being proportional to the costs of resistance. However, this evolutionary dynamic is open to modification by other sources of selection acting on the relative fitness of susceptible and resistant individuals. Here we show parasitism not only as a source of selection capable of modifying the costs of organophosphate insecticide resistance in mosquitoes, but also that qualitatively different interactions (increasing or decreasing the relative fitness of resistant individuals) occurred depending on the particular form of resistance involved. As estimates of the parasite's fitness also varied according to its host's form of resistance, our data illustrate the potential for epidemiological feedbacks to influence the strength and direction of selection acting on resistance mutations in untreated environments.