Archaea produce [FeFe] hydrogenases, previously thought to be exclusive to bacteria and eukaryotes. These enzymes are diverse, ranging from ultraminimal fermentative enzymes to ancient hybrid complexes, and have significant biotechnological potential. This study shows that anaerobic archaea encode active, diverse, and ancient lineages of [FeFe] hydrogenases through genome analysis and biochemical experiments. Nine archaeal phyla encode [FeFe] hydrogenases, and H2-producing Asgard archaeon cultures express these enzymes. An ultraminimal hydrogenase in DPANN archaea binds the catalytic H-cluster and produces H2. Hybrid complexes formed by the fusion of [FeFe] and [NiFe] hydrogenases are identified in ten archaeal orders. Phylogenetic analysis and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations of archaea, streamlined H2 catalysts for biotechnological development, and an intertwined evolutionary history between the two major H2-metabolizing enzymes. The study also shows that [FeFe] hydrogenases are active in archaea, with some archaea encoding functional [FeFe] hydrogenases. The study highlights the catalytic activity of [FeFe] hydrogenases and their potential for biotechnological applications. The findings suggest that [FeFe] hydrogenases have been acquired by archaea multiple times and have an ancient association with [NiFe] hydrogenases. The study also reveals the evolutionary history of [FeFe] hydrogenases, showing that they are diverse and ancient in archaea. The study concludes that archaea have evolved remarkably disparate ways to use [FeFe] hydrogenases to adapt to anoxic environments.Archaea produce [FeFe] hydrogenases, previously thought to be exclusive to bacteria and eukaryotes. These enzymes are diverse, ranging from ultraminimal fermentative enzymes to ancient hybrid complexes, and have significant biotechnological potential. This study shows that anaerobic archaea encode active, diverse, and ancient lineages of [FeFe] hydrogenases through genome analysis and biochemical experiments. Nine archaeal phyla encode [FeFe] hydrogenases, and H2-producing Asgard archaeon cultures express these enzymes. An ultraminimal hydrogenase in DPANN archaea binds the catalytic H-cluster and produces H2. Hybrid complexes formed by the fusion of [FeFe] and [NiFe] hydrogenases are identified in ten archaeal orders. Phylogenetic analysis and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations of archaea, streamlined H2 catalysts for biotechnological development, and an intertwined evolutionary history between the two major H2-metabolizing enzymes. The study also shows that [FeFe] hydrogenases are active in archaea, with some archaea encoding functional [FeFe] hydrogenases. The study highlights the catalytic activity of [FeFe] hydrogenases and their potential for biotechnological applications. The findings suggest that [FeFe] hydrogenases have been acquired by archaea multiple times and have an ancient association with [NiFe] hydrogenases. The study also reveals the evolutionary history of [FeFe] hydrogenases, showing that they are diverse and ancient in archaea. The study concludes that archaea have evolved remarkably disparate ways to use [FeFe] hydrogenases to adapt to anoxic environments.