In order to investigate the link between the methane dynamics in permafrost deposits and climate changes in the past, we studied the abundance, composition, and methane production of methanogenic communities in Late Pleistocene and Holocene sediments of the Siberian Arctic. We detected intervals of increased methane concentrations in Late Pleistocene and Holocene deposits along a 42 ka old permafrost sequence from Kurungnakh Island in the Lena Delta (northeast Siberia). Increased amounts of archaeal life markers (intact phospholipid ethers) and a high variety in genetic fingerprints detected by 16S ribosomal ribonucleic acid gene analyses of methanogenic archaea suggest presently living and presumably active methanogenic archaea in distinct layers predominantly in Holocene deposits, but also in deep frozen ground at 17 m depth. Potential methanogenic activity was confirmed by incubation experiments. By comparing methane concentrations, microbial incubation experiments, gene analysis of methanogens, and microbial life markers (intact phospholipid esters and ethers) to already partly degraded membrane lipids, such as archaeol and isoprenoid glycerol dialkyl glycerol tetraethers, we demonstrated that archaeol likely represents a signal of past methanogenic archaea. The archaeol signal was used to reconstruct the response of methanogenic communities to past temperature changes in the Siberian Arctic, and the data suggest higher methane emissions occurred during warm periods, particularly during an interval in the Late Pleistocene and during the Holocene. This new data on present and past methanogenic communities in the Siberian terrestrial permafrost imply that these microorganisms will respond to the predicted future temperature rise in the Arctic with increasing methane production, as demonstrated in previous warmer periods.