Despite the important effects of diet and parasite infection on male reproductive behavior, few studies have simultaneously addressed their influence on intrasexual selection (male--male competition). We examined the synergistic effects of 2 naturally varying environmental factors, lifetime food intake and infection, with the monogenean parasite Gyrodactylus turnbulli on the mating tactics and foraging behavior of male guppies (Poecilia reticulata). We allowed fish to interact directly with each other during observations and found that unparasitized males won more intermale contests, courted females more frequently, and received positive responses to courtship displays more frequently than males that had been infected. Infected males devoted more time to foraging and less time to courtship and competition than uninfected males, suggesting that they were energetically limited and could not increase reproductive effort despite their reduced expected lifespan. This interpretation was supported by the observation that greater food intake ameliorated the negative effects of parasite infection on courtship effort. Our results have bearing on how natural variation in food availability and parasite prevalence influence geographic variation in reproductive behavior. Copyright 2009, Oxford University Press.