The restoration of peatlands is an important strategy to counteract subsidence and loss of biodiversity. However, responses of important microbial soil processes are poorly understood. We assessed functioning, diversity and spatial organization of methanotrophic communities in drained and rewetted peat meadows with different water table management and agricultural practice. Results show that the methanotrophic diversity was similar between drained and rewetted sites with a remarkable dominance of the genus Methylocystis. Enzyme kinetics depicted no major differences, indicating flexibility in the methane (CH4) concentrations that can be used by the methanotrophic community. Short-term flooding led to temporary elevated CH4 emission but to neither major changes in abundances of methane-oxidizing bacteria (MOB) nor major changes in CH4 consumption kinetics in drained agriculturally used peat meadows. Radiolabeling and autoradiographic imaging of intact soil cores revealed a markedly different spatial arrangement of the CH4 consuming zone in cores exposed to near-atmospheric and elevated CH4. The observed spatial patterns of CH4 consumption in drained peat meadows with and without short-term flooding highlighted the spatial complexity and responsiveness of the CH4 consuming zone upon environmental change. The methanotrophic microbial community is not generally altered and harbors MOB that can cover a large range of CH4 concentrations offered due to water-table fluctuations, effectively mitigating CH4 emissions.