Updated project metadata. Methane-generating Archaea drive the final step in anaerobic organic compound mineralization and dictate the carbon flow of Earth’s diverse anaerobic ecosystems. Although such Archaea were presumed to be restricted to life on simple compounds like H2, acetate or methanol, an archaeon, Methermicoccus shengliensis, was recently found to convert methoxylated aromatic compounds to methane. Methoxylated aromatic compounds as component of lignin and coal are present in most subsurface sediments. Despite the significance and novelty of this outstanding archaeon its metabolism has not yet been explored. In this study, transcriptomics and proteomics reveal that M. shengliensis uses a demethoxylation system that is more related to that from acetogenic bacteria than to the methyl transferase system used for methylotrophic methanogenesis. It activates methoxy-groups using tetrahydromethanopterin as the carrier, a mechanism distinct from conventional methanogenic methyl-transfer systems dependent on Coenzyme M.