Molecular hydrogen (H2) is a widespread, energetically efficient reductant supporting microbial metabolism across most known ecosystems. Although seafloor hydrothermal vents are major energy providers for H2-oxidizing microorganisms, the diversity of H2 oxidation potential in H2-rich systems remains poorly constrained. Here, we use a metagenomic approach to, for the first time, assess the genome-resolved microbial energy conservation potential within hydrothermal deposits and sediments from the ice-covered, extraordinarily H2-rich Aurora Vent Field in the Arctic Ocean. Community-wide analysis revealed broad taxonomic representation of microorganisms with the potential to consume H₂ for energy conservation. Notably, we report the first genome belonging to the cosmopolitan Zetaproteobacteria genus Mariprofundus encoding the capacity for H2 oxidation. Additionally, novel, highly abundant Aquificota at Aurora encode uptake hydrogenases not previously characterized as central to H2 oxidation at deep sea vents. The encoded gene content of abundant taxa points to a preference for flexible rather than obligate lithotrophic energy metabolism. A substantial fraction of inferred H₂-oxidizing potential is associated with presumed heterotrophs, potentially enhancing carbon transfer efficiency within the Aurora microbial food web. Overall, this study sheds new light on the importance of H2 availability for shaping microbial communities in hydrothermal systems.