Over billions of years, Archaea have adapted to a wide diversity of environments on Earth. During this time, one of the greatest challenges and opportunities was the rise of molecular oxygen within the atmosphere. Several archaeal lineages have independently evolved aerobic metabolisms across the Crenarchaeota, Thaumarchaeota, and Euryarchaeota. While the most distinctive archaeal group, methanogens, have generally retained their anaerobic metabolism, this pathway has been lost several times, in the cases of Halobacteriales, Thermoplasmatales, and Archaeoglobales. Each of these lineages has a metabolism that either directly or indirectly depends on the presence of molecular oxygen within the environment, suggesting that these transitions were in response to rising oxygen levels. We map the history of oxygen tolerance across these groups via phylogeny of a gene encoding the superoxide dismutase (SOD) enzyme, which detoxifies free radical oxygen species. We find that this gene was independently acquired via HGT many times within Archaea, especially within aerobic groups. These acquisitions appear to be singular adaptive events, without subsequent transfers or losses after the initial acquisitions. We propose that these transfers document the rising levels of oxygen across environments, with the earliest acquisitions immediately following the Great Oxygenation Event, and subsequent, more recent transfers tied to higher levels of oxygen experienced since the Neoproterozoic. The evolutionary history of additional oxygen-associated gene families in Archaea will further assist in reconstructing this narrative of the oxygenation of the microbial world.