Methlymercury is a significant risk to environmental health globally. We examined the ecological drivers of methylmercury bioaccumulation in songbirds and its effect on body condition while experimentally removing the potentially confounding and predominant effects of site and habitat. We measured blood and feather mercury concentrations and body condition in nearly 1200 individuals representing resident or migrant songbirds of 52 species and 5 foraging guilds. Songbird mercury concentrations differed among species, foraging guilds, residency status, dates, and ages, but not sexes. Blood mercury concentrations 1) ranged from 0.003 in house finch to 0.85 μg/g ww in American robin, 2) were 125 times greater in insectivores than granivores and 3.6 times greater in insectivores than omnivores, 3) were 3.3 times greater in summer residents than in migrating songbirds, 4) increased by 25% throughout spring and summer, and 5) were 45% higher in adults than juveniles. Songbird mercury concentrations were negatively correlated with body condition, with blood mercury concentrations decreasing by 44% and 34% over the range of standardized body masses and fat scores, respectively. Our results highlight the importance of foraging and migration ecology in determining methylmercury contamination in birds, and the potential for reduced body condition with methylmercury exposure in songbirds.