Methane oxidizing bacteria (methanotrophs) within the genus Methylobacter constitute the biological filter for methane (CH4) in many Arctic soils. Multiple Methylobacter strains have been identified in these environments but we seldom know the ecological significance of the different strains. High-Arctic peatlands in Svalbard are heavily influenced by herbivory, leading to reduced vascular plant and root biomass. Here, we have measured potential CH4 oxidation rates and identified the active methantrophs in grazed peat and peat protected from grazing by fencing (exclosures) for 18 years. Grazed peat sustained a higher water table, higher CH4 concentrations and lower oxygen (O2) concentrations than exclosed peat. Correspondingly, the highest CH4 oxidation potentials were closer to the O2 rich surface in the grazed than in the protected peat. A comparison of 16S rRNA genes showed that the majority of methanotrophs in both sites belong to the genus Methylobacter. Further analyses of pmoA transcripts revealed that several Methylobacter OTUs were active in the peat but that different OTUs dominated the grazed peat than the exclosed peat. We conclude that grazing influences soil conditions, the active CH4 filter and that different Methylobacter populations are responsible for CH4 oxidation depending on the environmental conditions.