If ornament quality advertises heritable resistance to a directly transmitted parasite, female preference for males with higher quality ornaments could reduce parasite prevalence via two pathways. Preference for, and thus more contact with, resistant males should: 1) change parasite transmission opportunities; and 2) increase offspring parasite resistance. Here, we used data and parameterized a SIR model to test the hypothesis that, across populations of guppies (Poecilia reticulata), the strength of female preference negatively correlates with prevalence of directly transmitted gyrodactylids. Female guppies exhibit between-population variation in preference for males with larger orange ornaments that are heritable and forecast resistance. Using 89 prevalence estimates from 10 populations, and controlling for ecological covariates, we found that populations with significant female preference had lower prevalence than those without. Our theoretical model inferred that preference affects prevalence largely by affecting offspring parasite resistance. Female preference can thus drive the dynamics of ordinary infectious diseases.