Fleas (Insecta: Siphonaptera) are hematophagous ectoparasites that feed on vertebrate hosts. Fleas can reduce the fitness of hosts by interfering with immune responses, disrupting adaptive behaviors, and transmitting pathogens. The negative effects of fleas on hosts are usually most pronounced when fleas attain high densities. In lab studies, fleas desiccate and die under dry conditions, suggesting that populations of fleas will tend to decline when precipitation is scarce under natural conditions. To test this hypothesis, we compared precipitation vs. parasitism of black-tailed prairie dogs (Cynomys ludovicianus) by fleas at a single colony during May and June of 13 consecutive years (1976–1988) at Wind Cave National Park, South Dakota, USA. The number of fleas on prairie dogs decreased with increasing precipitation during both the prior growing season (April through August of the prior year) and the just-completed winter–spring (January through April of current year). Due to the reduction in available moisture and palatable forage in dry years, herbivorous prairie dogs might have been food-limited, with weakened behavioral and immunological defenses against fleas. In support of this hypothesis, adult prairie dogs of low mass harbored more fleas than heavier adults. Our results have implications for the spread of plague, an introduced bacterial disease, transmitted by fleas, that devastates prairie dog colonies and, in doing so, can transform grassland ecosystems.