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Contaminants in harvested species can pose serious concerns for health and food security. However, the risks of contaminant exposure can be challenging to track as many species migrate extensively between breeding and feeding environments and usually form genetically distinct populations. Such intraspecific complexity may translate into variation in exposure and bioaccumulation. We firstly investigated the genetic structure and the mixed-stock fishery origin of migratory Walleye (Sander vitreus) and Lake Whitefish (Coregonus clupeaformis) samples harvested from western Lake Athabasca and the Peace-Athabasca Delta (Alberta, Canada), using species-specific panels of single nucleotide polymorphisms (SNPs; n = 211-357 loci). We then explored which variables impacted mercury concentration in fish muscle tissue, including breeding (distinct populations) and feeding environments (fishery capture location). We identified two genetically distinct populations in each species whose harvest proportions differed between the lake and delta. In both species, the population spawning in the river upstream of, and migrating through the Alberta Oil Sands was exposed to higher mercury levels. In Walleye, this translated into 65 % more mercury than in the second population, with 43 % of individuals exceeding Health Canada recommended levels for human consumption. In Whitefish, river spawners, which were much younger and contributed more the harvest, had higher mercury concentrations than lake spawners when controlling for age. We also found different relationships between mercury and individual heterozygosity or body condition among populations. Collectively, our results reveal varying mercury loads at the population level in two fishes with widespread importance for fisheries, highlighting the utility of genetic-based monitoring to better understand contaminants.