Archaea have been found to encode diverse and active [FeFe] hydrogenases, challenging the previous belief that these enzymes were restricted to bacteria and eukaryotes. The study combines genome analysis with biochemical experiments to demonstrate that nine archaeal phyla encode structurally diverse [FeFe] hydrogenases. Notably, uncultured DPANN archaea produce ultraminimal [FeFe] hydrogenases that bind the catalytic H-cluster and produce H₂. Additionally, ancient hybrid complexes formed by the fusion of [FeFe] and [NiFe] hydrogenases are identified in ten other archaeal orders. Phylogenetic and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations in archaea, streamlined H₂ catalysts for biotechnological development, and an intertwined evolutionary history between the two major H₂-metabolizing enzymes. The study also highlights the potential of combining genome-resolved metagenomics with protein structure prediction and heterologous production studies to discover new enzymes and functions in uncultured microorganisms.Archaea have been found to encode diverse and active [FeFe] hydrogenases, challenging the previous belief that these enzymes were restricted to bacteria and eukaryotes. The study combines genome analysis with biochemical experiments to demonstrate that nine archaeal phyla encode structurally diverse [FeFe] hydrogenases. Notably, uncultured DPANN archaea produce ultraminimal [FeFe] hydrogenases that bind the catalytic H-cluster and produce H₂. Additionally, ancient hybrid complexes formed by the fusion of [FeFe] and [NiFe] hydrogenases are identified in ten other archaeal orders. Phylogenetic and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations in archaea, streamlined H₂ catalysts for biotechnological development, and an intertwined evolutionary history between the two major H₂-metabolizing enzymes. The study also highlights the potential of combining genome-resolved metagenomics with protein structure prediction and heterologous production studies to discover new enzymes and functions in uncultured microorganisms.