The microbial community in peat is responsible for organic matter degradation and greenhouse gas emissions, yet its response to peat extraction and peatland restoration remains poorly understood. We investigated how different physicochemical conditions in natural, restored, unrestored, and actively extracted peatlands influenced the methanogenic and methanotrophic community characteristics. 16S rRNA amplicon sequencing allowed for the comparison of the abundance of both groups. The communities were similar at sites restored in 1991 and 2009 (25 and 7 years prior to our research) that had high water table and were dominated by sedges. A different, shared pattern of microbial membership was observed at natural, unrestored, and actively extracted sites, and a site restored in 2012 (4 years prior to the research). These similarities were reflected in peat chemistry and hydrology in canonical correspondence analysis (CCA) ordination that was used to investigate how these factors affected the abundances of methane cycling taxa. Based on the CCA, methanotrophs reached their highest abundances close to the water table, at high and moderate concentrations of phosphate and propionate, and low concentrations of formate. Methanogens exhibited a more distributed pattern, with organisms responding to opposite conditions along these environmental gradients. Methane-cycling community in older restored sites departed from the reference community at the natural bog likely due to the fen-like conditions that developed at these sites.