Permafrost thaw could increase methane (CH₄) emissions, which largely depends on CH₄ production driven by methanogenic archaea. However, large-scale evidence regarding key methanogenic taxa and their relative importance to abiotic factors in mediating methanogenesis remains limited. Here, we explored the methanogenic community, potential CH₄ production and its determinants in the active layer and permafrost deposits based on soil samples acquired from 12 swamp meadow sites along a ～1000 km permafrost transect on the Tibetan Plateau. Our results revealed lower CH₄ production potential, mcrA gene abundance, and richness in the permafrost layer than those in the active layer. CH₄ production potential in both soil layers was regulated by microbial and abiotic factors. Of the microbial properties, marker OTUs, rather than the abundance and diversity of methanogens, stimulated CH₄ production potential. Marker OTUs differed between the two soil layers with hydrogenotrophic Methanocellales and facultative acetoclastic Methanosarcina predominant in regulating CH₄ production potential in the permafrost and active layer, respectively. Besides microbial drivers, CH₄ production potential increased with the carbon/nitrogen (C/N) ratio in both soil layers and was also stimulated by soil moisture in the permafrost layer. These results provide empirical evidence for model improvements to better predict permafrost carbon feedback to climate warming.