Fisheries in highly productive prairie lakes of Canada and the USA frequently have fish consumption advisories due to elevated mercury concentrations. This occurrence is unexpected because such alkaline lakes often exhibit lower methylmercury (MeHg) concentrations in basal trophic levels than those expected in less productive basins with circumneutral pH. As sources of MeHg to fish are largely dietary, components of the food web are expected to be critical controls of the transfer of MeHg to fish. Here we investigated how Leptodora kindtii, a large (1.5 cm) translucent predatory invertebrate that exhibits pronounced diel vertical migration (in sediments by day, upper water column by night) plays a key role in regulating the contamination of fish with MeHg in a well-studied, eutrophic, prairie lake in western Canada. Estimates of diel fluxes of invertebrate biomass and MeHg revealed that migratory adult Leptodora, but not other adult zooplankton or juvenile Leptodora, acted as a vector, uniquely transferring MeHg from presumptive deepwater sites of methylation to pelagic fish communities. This cryptic process suggests that piscivorous fish may experience greatly elevated exposure to MeHg even in circumstances when biogeochemical features, MeHg sources, and daytime food-web configuration suggest that trophic transfers should be minimal.