Animals inhabiting urban areas often experience elevated disease threats, putatively due to factors such as increased population density and horizontal transmission or decreased immunity (e.g. due to nutrition, pollution, stress). However, for animals that take advantage of human food subsidies, like feeder-visiting birds, an additional mechanism may include exposure to contaminated feeders as fomites. There are some published associations between bird feeder presence/density and avian disease, but to date no experimental study has tested the hypothesis that feeder contamination can directly impact disease status of visiting birds, especially in relation to the population of origin (i.e. urban v. rural, where feeder use/densities naturally vary dramatically). Here we used a field, feeder-cleaning experimental design to show that rural, but not urban, house finches (Haemorhous mexicanus) showed increased infection from a common coccidian endoparasite (Isospora spp.) when feeders were left uncleaned and that daily cleaning (with diluted bleach solution) over a 5-week period successfully decreased parasite burden. Moreover, this pattern in rural finches was true for males but not females. These experimental results reveal habitat- and sex-specific harmful effects of bird feeder use (i.e. when uncleaned in rural areas). Our study is the first to directly indicate to humans who maintain feeders for granivorous birds that routine cleaning can be critical for ensuring the health and viability of visiting avian species.