Many methanogens in the digestive tract of animals fall into the radiation of the genus Methanobrevibacter. Recent studies revealed that the genus Methanobrevibacter is underclassified and comprises numerous genus-level lineages. Based on a comprehensive phylogenomic analysis, which includes all uncultured representatives with sequenced genomes and considers the relative evolutionary divergence of individual lineages, we propose seven new genera (type species in parentheses). While Methanacia gen. nov. (M. filiformis comb. nov.), Methanobaculum gen. nov. (M. cuticularis comb. nov.), Methanobinarius gen. nov. (M. arboriphilus comb. nov.), and Methanoflexus gen. nov. (M. curvatus comb. nov.) are found almost exclusively in the digestive tract of insects and millipedes, Methanobrevibacter sensu stricto, Methanarmilla gen. nov. (M. wolinii comb. nov.) and Methanocatella gen. nov. (M. smithii comb. nov.) harbor all isolates from mammals and birds. Two additional lineages from termites ("Methanorudis" and "Methanovirga") are without cultured representatives. The representatives from arthropods and vertebrates form two distinct clades that show patterns of coevolution with their respective host groups. An exception is Methanomonila gen. nov. (M. shimae sp. nov.), whose members occur arthropods but are sister to the genus Methanocatella from vertebrates. The only isolate is strain Ec1 from the cockroach Ergaula capucina, a hydrogenotrophic methanogen that reduces CO2 with H2 or formate. Based on these results, we conclude that an association with animals occurred twice in the evolutionary history of the order Methanobacteriales, once in the ancestor of the Methanobrevibacter sensu lato supercomplex, and once during the radiation of the Methanobacterium supercomplex (i.e., in the genus Methanosphaera).