Ombrotrophic peatlands are a recognized global carbon reservoir. Without restoration and peat regrowth, harvested peatlands are dramatically altered, impairing its carbon sink function, with consequences for methane turnover. Previous studies determined the impact of commercial mining on the peat physico-chemical properties, and the effects on methane turnover. However, the response of the underlying microbial communities catalyzing methane production and oxidation have so far received little attention. We hypothesize that with the return of Sphagnum post-harvest, methane turnover potentials and the corresponding microbial communities will converge in a natural and restored peatland. To address our hypothesis, we determined the potential methane production and oxidation rates in a natural (as a reference), actively mined, abandoned, and restored peatland over two consecutive years. In all sites, the methanogenic and methanotrophic population size were enumerated using qPCR assays targeting the mcrA and pmoA genes, respectively. Shifts in the community composition was determined using Illumina MiSeq sequencing of the mcrA gene, and a pmoA-based t-RFLP analysis, complemented by cloning and sequence analysis of the mmoX gene. Peat mining adversely affected methane turnover potentials, but rates recovered in the restored site. The recovery in potential activity was reflected in the methanogenic and methanotrophic abundances. However, the microbial community composition was altered, more pronounced for the methanotrophs. Overall, we observed a lag between the recovery of the methanogenic/methanotrophic activity and the return of the corresponding microbial communities, suggesting a longer duration (>15 years) is needed to reverse mining-induced effects on the methane-cycling microbial communities.