Plague is a bacterial zoonosis of mammalian hosts and flea vectors. The disease is capable of ravaging rodent populations and transforming ecosystems. Because plague mortality is likely to be predicted by flea parasitism, it is critical to understand vector dynamics. It has been hypothesized that paltry precipitation and reduced vegetative production predispose herbivorous rodents to malnourishment and flea parasitism, and flea parasitism varies directly with plague mortality. We evaluated these hypotheses on five colonies of Utah prairie dogs (UPDs; Cynomys parvidens), on the Awapa Plateau, Utah, US, in 2013–16. Ten flea species were identified among 3,257 fleas from UPDs. These 10 flea species parasitize prairie dogs, mice, rats, voles, ground squirrels, chipmunks, and marmots, all known hosts of plague. The abundance of fleas on individual UPDs (1,198 observations) varied inversely with UPD body condition; fleas were most abundant on lightweight, malnourished UPDs. Flea abundance on UPDs was highest in dry years that were preceded by wet years. Increased precipitation and soil moisture in the prior year might generate humid microclimates in UPD burrows (that could facilitate flea survival and reproduction) and paltry precipitation in the current year could predispose UPDs to malnourishment and flea parasitism. Annual re-encounter rates for UPDs (1,072 observations) were reduced in wetter years preceded by drier years; reduced precipitation and vegetative production might kill UPDs, and increased flea densities in drier years could provide conditions for plague transmission (and UPD mortality) when moisture returns. Re-encounter rates were reduced for UPDs carrying at least one flea compared to UPDs with no detected fleas. These results support the hypothesis that reduced precipitation in the current year predisposes UPDs to flea parasitism. Our results also suggest a link between flea parasitism and UPD mortality. Given documented connections between flea parasitism and plague transmission, our results point toward an effect of flea parasitism on plague-related deaths for individual UPDs, a phenomenon rarely investigated in nature.