Despite their large environmental impact and multiple independent emergences, the processes leading to the evolution of anaerobic methanotrophic archaea (ANME) remain unclear. This work uses comparative metagenomics of a recently evolved but understudied ANME group, “
Candidatus
Methanovorans” (ANME-3), to identify evolutionary processes and innovations at work in ANME, which may be obscured in earlier evolved lineages. We identified horizontal transfer of
hdrA
homologs and convergent evolution in carbon and energy metabolic genes as potential early steps in
Methanovorans
evolution. We also identified the erosion of genes required for methylotrophic methanogenesis along with horizontal acquisition of multiheme cytochromes and other loci uniquely associated with ANME. The assembly and comparative analysis of multiple
Methanovorans
genomes offers important functional context for understanding the niche-defining metabolic differences between methane-oxidizing ANME and their methanogen relatives. Furthermore, this work illustrates the multiple evolutionary modes at play in the transition to a globally important metabolic niche.