We investigated the dietary pathways of mercury transfer in the food web of Morency Lake (Canada) to determine the influence of carbon source and habitat use on mercury bioaccumulation in fish. Whole-body concentrations of methylmercury (MeHg) were significantly different in four fish species (white sucker, brown bullhead, pumpkinseed and smallmouth bass) and increased with both trophic position and greater feeding on offshore (versus littoral) carbon. An examination of fish gut contents and the depth distribution of invertebrates in Morency Lake showed that smallmouth bass and brown bullhead were supplementing their littoral diet with the consumption of either opossum shrimp (Mysis diluviana) or profundal amphipods in offshore waters. The zooplanktivore Mysis had significantly higher MeHg concentrations than zooplankton and benthic invertebrates, and it was an elevated source of MeHg to smallmouth bass. In contrast, profundal amphipods consumed by brown bullhead did not have higher MeHg concentrations than littoral amphipods. Instead, partitioning of benthic invertebrate resources likely explains the greater MeHg bioaccumulation in brown bullhead, associated with offshore feeding of amphipods. White sucker and brown bullhead had a similar trophic position but white sucker consumed more chironomids, which had one-third the MeHg concentration of amphipods. Our findings suggest that offshore feeding in a lake can affect fish MeHg bioaccumulation via two different processes: (1) the consumption of MeHg-enriched pelagic prey, or (2) resource partitioning of benthic primary consumers with different MeHg concentrations. These observations on the mechanisms of habitat-specific bioaccumulation highlight the complexity of MeHg transfer through lake food webs.