Single carbon (C1) compounds such as methanol, methylamines and formaldehyde are ubiquitous in nature and they are large components of the carbon cycle. In anoxic environments C1-utilizing microbes (methylotrophs) play an important role in controlling global carbon degradation. Currently described anaerobic methylotrophs are limited to methanogenic archaea, acetogenic bacteria, and sulfate-reducing bacteria. Here, we report the first archaeal lineage outside of methanogenic taxa that are capable of anaerobic methylotrophy. Phylogenetic analyses suggest these archaea form a new phylum within the TACK superphylum, which we propose be named Brockarchaeota. A survey revealed Brockarchaeota are globally distributed in geothermal springs. Metabolic inference from 15 metagenome-assembled genomes from hot springs and deep-sea sediments indicates that Brockarchaeota are strict anaerobes. They contain a variety C1 metabolisms including the methanol and trimethylamine methyltransferases system, the ribulose bisphosphate pathway coupled with the non-oxidative pentoses phosphate pathway, and reductive glycine pathway. Brockarchaeota have an incomplete methyl-branch of the Wood-Ljungdahl pathway probably used for formaldehyde oxidation, since they lack several core genes involved in methanogenesis including methyl-CoM reductases. Brockarchaeota also appear to play an important role in the breakdown of plant-derived polysaccharides, especially cellulose, starch and xylan. Their broad distribution and their capacity to use both C1 compounds and complex polysaccharides via anaerobic metabolism suggest that the Brockarchaeota occupy previously overlooked roles in carbon cycling.