The release of carbon from newly thawed permafrost is estimated to add between 0.05 and 0.39 °C to the simulated global mean surface air temperature by the year 2300. The release of the potent greenhouse gas CH4 following permafrost thaw is thereby of particular concern. Models simulated a contribution of CH4 to the radiative forcing from thawing permafrost of up to 40% for the maximum extent of thermokarst. Batch experiments on thawed permafrost samples, however, have rendered the contribution of anaerobically produced carbon and in particular of CH4 to be surprisingly weak and CH4 production which is realized through methanogenic archaea was reported to be low and associated with long lag phases . This leads to the hypotheses that initial methanogenic population sizes and/or substrates are limiting factors in permafrost. The objective of this study is to identify constraints for CH4 production in thawing permafrost. We analyzed several low Arctic permafrost cores of up to 3 m depth of different land cover types, sediment properties, age and stratigraphy for methanogenic abundance, potential methane production and predictors of both. We found that methanogenic population size and substrate pool are constraints on methane production but unlike expected, they do not fully explain low CH4 production rates in thawing permafrost. Even when both, population size and substrate concentrations, were large, the potential production of CH4 was still comparably low. Furthermore we show that the potential production of CH4 in thawing permafrost is a function of the methanogenic population size if substrate is not the limiting factor and that the methanogenic population size in turn is a function of the carbon density. Based on our study we propose that on the long term after permafrost has thawed, growth and community shifts within the methanogenic population will occur which potentially will increase methane production by orders of magnitude.