Global pollution of mercury (Hg) threatens ecosystem and human health. We measured total Hg (THg) and monomethylmercury (MMHg) concentrations in filter-feeding blackfly (Simulium spp.) larvae in the inflows and the outflows of six boreal lakes with no Hg point source pollution. THg in the larvae ranged from 0.03 to 0.31 mg kg−1 dw and MMHg between 0.02 and 0.25 mg kg−1 dw. The proportion of MMHg in the larvae was 74 ± 0.16% and ranged from 43 to 98% of THg, the highest proportions being comparable to those typically found in aquatic predatory insects and fish. We compared the larvae MMHg concentrations to river water quality, catchment land-use, and to size-adjusted lake pike THg data. Two of the investigated catchments have been affected by a multimetal biomine since 2008 and were characterized by higher conductivity and higher urban land-use activity. Larvae THg and MMHg concentrations were higher in the lake inflows than in outflows and associated with water conductivity and catchment land-use activity. Lake pike THg concentrations were highly correlated to lake outflow blackfly larvae MMHg concentrations. Our data illustrate that blackfly larvae take up high percentage of THg that is MMHg, which in turn is available for higher consumers in aquatic and terrestrial food webs.