Hydrothermally influenced sediments are among the most dynamic interfaces in the deep ocean, where steep redox gradients, hydrothermal inputs, and sediment-water exchange sustain exceptionally diverse microbial communities that drive global carbon and nutrient cycling. Yet the metabolic potential and evolutionary diversity of these ecosystems remain poorly resolved because much of their microbial life belongs to uncultivated and deeply branching lineages. Here, we combine large-scale genome-resolved metagenomics with comparative analyses across hydrothermal sediments to provide a comprehensive view of microbial diversity and metabolism in the deep seafloor. We reconstructed more than 9,000 metagenome-assembled genomes from 40 sediment samples spanning hydrothermal gradients in Guaymas Basin, including over 2,000 archaeal genomes representing 123 phyla and hundreds of previously undescribed higher taxonomic groups. These data substantially expand the known diversity of key metabolic proteins involved in methane, hydrogen, sulfur, and C1 compound transformations, nearly doubling the known sequence diversity of hydrogenases and revealing widespread capacities for methylotrophy across abundant uncultivated lineages. Beyond expanding genomic diversity, these datasets uncover previously unrecognized microbial groups and metabolic strategies that reshape our understanding of deep-sea ecosystem functioning. Comparative analyses reveal extensive metabolic innovation across newly described bacterial and archaeal phyla, including lineages involved in hydrocarbon degradation, sulfur transformations, carbon fixation, and oxygen metabolism. In particular, genomes from Asgard archaea illuminate the evolutionary history of aerobic metabolism in descendants of the archaeal ancestor of eukaryotes, while numerous newly discovered bacterial lineages broaden the phylogenetic distribution of pathways central to carbon and energy conservation. By linking evolutionary history with microbial function across environmental gradients, this work provides a new framework for understanding how benthic microbial communities regulate elemental cycling and influence the functioning of the deep ocean.