Diverse aerobic bacteria use atmospheric hydrogen (H2) and carbon monoxide (CO) as energy sources for growth and survival. Hydrogenases and CO dehydrogenases input the electrons derived from these trace gases into the aerobic respiratory chain. Though recently discovered, trace gas oxidation is now recognised as a globally significant process that serves as the main sink in the biogeochemical H2 cycle and sustains microbial biodiversity in oligotrophic ecosystems. Though trace gas oxidation has been reported in nine phyla of bacteria, it is unclear whether the domain archaea are also capable of using atmospheric H2. Here we show that a thermoacidophilic archaeon, Acidianus brierleyi (phylum Thermoproteota), constitutively consumes H2 and CO to sub-atmospheric levels. Oxidation occurred during both growth and survival across a wide range of temperatures (10 to 70°C). Genomic analysis demonstrated that A. brierleyi encodes a canonical CO dehydrogenase and, unexpectedly, four distinct [NiFe]-hydrogenases from subgroups not known to mediate aerobic H2 uptake. Quantitative proteomic analyses showed that A. brierleyi differentially produced these enzymes in response to electron donor and acceptor availability. A previously unidentified group 1 [NiFe]-hydrogenase with a unique genetic arrangement is constitutively expressed and upregulated under stationary phase and aerobic hydrogenotrophic growth. Integrating these findings, continual harvesting of atmospheric trace gases likely drives niche expansion of A. brierleyi, including survival during dispersal through temperate environments. These results prove that atmospheric H2 consumption is a cross-domain phenomenon, suggest an ancient origin of this trait, and identify previously unknown microbial and enzymatic sinks of atmospheric H2 and CO.