Drained peatlands are significant sources of the greenhouse gas (GHG) carbon dioxide. Rewetting is a proven strategy used to protect carbon stocks; however, it can lead to increased emissions of the potent GHG methane. The response to rewetting of soil microbiomes as drivers of these processes is poorly understood, as are the biotic and abiotic factors that control community composition. We analyzed the pro- and eukaryotic microbiomes of three contrasting pairs of minerotrophic fens subject to decade-long drainage and subsequent long-term rewetting. Abiotic soil properties including moisture, dissolved organic matter, methane fluxes, and ecosystem respiration rates were also determined. The composition of the microbiomes was fen-type-specific, but all rewetted sites showed higher abundances of anaerobic taxa compared to drained sites. Based on multi-variate statistics and network analyses, we identified soil moisture as a major driver of community composition. Furthermore, salinity drove the separation between coastal and freshwater fen communities. Methanogens were more than 10-fold more abundant in rewetted than in drained sites, while their abundance was lowest in the coastal fen, likely due to competition with sulfate reducers. The microbiome compositions were reflected in methane fluxes from the sites. Our results shed light on the factors that structure fen microbiomes via environmental filtering.