Mercury is a ubiquitous metal contaminant that negatively impacts reproduction of wildlife and has many other sub-lethal effects. Songbirds are sensitive bioindicators of mercury toxicity and may suffer population declines as a result of mercury pollution. Current predictions of mercury accumulation and biomagnification often overlook possible genetic variation in mercury uptake and elimination within species and the potential for evolution in affected populations. We conducted a study of dietary mercury exposure in a model songbird species, maintaining a breeding population of zebra finches (Taeniopygia guttata) on standardized diets ranging from 0.0–2.4 μg/g methylmercury. We applied a quantitative genetics approach to examine patterns of variation and heritability of mercury accumulation within dietary treatments using a method of mixed effects modeling known as the 'animal model'. Significant variation in blood mercury accumulation existed within each treatment for birds exposed at the same dietary level; moreover, this variation was highly repeatable for individuals. We observed substantial genetic variation in blood mercury accumulation for birds exposed at intermediate dietary concentrations. Taken together, this is evidence that genetic variation for factors affecting blood mercury accumulation could be acted on by selection. If similar heritability for mercury accumulation exists in wild populations, selection could result in genetic differentiation for populations in contaminated locations, with possible consequences for mercury biomagnification in food webs.