Abstract. Microbial communities of methane (CH4) producing methanogens and consuming methanotrophs play an important role for Earth's atmospheric CH4 budget. Despite their global significance, knowledge on how much they control the spatial variation in CH4 fluxes from peatlands is poorly understood. We studied variation in CH4 producing and consuming communities in a natural peatland dominated by Eriophorum vaginatum, via a metagenomics approach using custom designed hybridization-based oligonucleotide probes to focus on taxa and functions associated with methane cycling. We hypothesized that sites with different magnitudes of methane flux are occupied by structurally and functionally different microbial communities, despite the dominance of a single vascular plant species. To investigate this, nine plant-peat mesocosms dominated by the sedge Eriophorum vaginatum, with varying vegetation coverage, were collected from a temperate natural wetland and subjected to a simulated growing season. During the simulated growing season, measurements of CH4 emission, carbon dioxide (CO2) exchange and δ13C signature of emitted CH4 were made. Mesocosms 1 through 9 were classified into three categories according to the magnitude of CH4 flux. Gross primary production and ecosystem respiration followed the same pattern as CH4 fluxes, but this trend was not observed in net ecosystem exchange. We observed that genetic functional potential was of minor importance in explaining spatial variability of CH4 fluxes with only small shifts in taxonomic community and functional genes. In addition, a higher β-diversity was observed in samples with high CH4 emission. Among methanogens, Methanoregula, made up over 50 % of the community composition. This, in combination with the remaining hydrogenotrophic methanogens matched the δ13C isotopic signature of emitted CH4. However, the presence of acetoclastic and methylotrophic taxa and type I, II and Verrucomicrobia methanotrophs indicates that the microbial community holds the ability to produce and consume CH4 in multiple ways. This is important in terms of future climate scenarios, where peatlands are expected to alter in nutrient status, hydrology, and peat biochemistry. Due to the high functional potential, we expect the community to be highly adaptive to future climate scenarios.