Small oxygen-stratified humic lakes of the boreal zone are important sources of methane to the atmosphere. Although stable isotope profiling has indicated that a substantial part of methane is already oxidized in the anaerobic water layers in these lakes, the contributions of aerobic and anaerobic methanotrophs in the process are unknown. We used next-generation sequencing of mcrA and 16S rRNA genes to characterize the microbial communities in the water columns of 2 boreal lakes in Finland, Lake Alinen-Mustajärvi and Lake Mekkojärvi, and complemented this with a shotgun metagenomic analysis from Alinen-Mustajärvi and an analysis of pmoA genes and 16S rRNA, mcrA, and pmoA transcripts from Mekkojärvi. Furthermore, we tested the effect of various electron acceptors and light on methane oxidation (13C-CH4 labeling) in incubations of water samples collected from the lakes. Aerobic gammaproteobacterial methanotrophs (order Methylococcales) exclusively dominated the methanotrophic community both above and below the oxycline in the lakes. A novel lineage within Methylococcales, Candidatus Methyloumidiphilus alinensis, defined here for the first time, dominated in Alinen-Mustajärvi, while methanotrophs belonging to Methylobacter were more abundant in Mekkojärvi. Light enhanced methane oxidation in the anoxic water layer, while alternative electron acceptors (SO4 2−, Fe3+, Mn4+, and anthraquinone-2,6-disulfonate), except for NO3 −, suppressed the process. Our results suggest that oxygenic photosynthesis potentially fuels methanotrophy below the aerobic water layers in methane-rich boreal lakes. Furthermore, incubation results, together with the detection of denitrification genes from metagenome-assembled genomes of gamma proteo - bacterial methanotrophs, imply that boreal lake methanotrophs may couple methane oxidation with NOx − reduction in hypoxic conditions.