The significance of methane production by lakes to the global production of greenhouse gas is well acknowledged while underlying processes sustaining the lacustrine methane budget remain largely unknown. We coupled biogeochemical data to functional and phylogenetic analyses to understand how sedimentary parameters characterize the methane cycle vertically and horizontally in the ice-covered bay of the second largest lake in Europe, Lake Onego, Russia. Our results support a heterogeneous winter methane cycle, with higher production and oxidation closest to riverine inputs. Close to the river mouth, the largest numbers of copies of methane-related functional genes pmoA and mcrA were associated with a specific functional community, and methane production potential exceeded oxidation, resulting in 6-10 times higher methane fluxes than in the rest of the bay. The elevated fluxes arise from the spatial differences in quantity and type (lacustrine versus riverine sources) of organic matter. More homogeneity is found toward the open lake, where the sediment is vertically structured into 3 zones: a shallow zone of methane oxidation; a transitional zone (5-10 cm) where anaerobic methane oxidation is dominant; and a methane production zone below. This vertical pattern is structured by the redox gradient and human-induced changes in sedimentary inputs to the bay. Retrieved 16S rRNA gene sequences from Candidatus Methanoperedens and Cand. Methylomirabilis suggest that anaerobic oxidation of methane occurs in these freshwater lake sediments.