Since the archaeal domain of life was first recognized, it has often been assumed that Archaea are ancient, and harbor primitive traits. In fact, the names of the major archaeal lineages reflect our assumptions regarding the antiquity of their traits. Ancestral state reconstruction and relaxed molecular clock analyses using newly articulated oxygen age constraints show that although the archaeal domain itself is old, tracing back to the Archean eon, many clades and traits within the domain are not ancient or primitive. Indeed many clades and traits, particularly in the Euryarchaeota, were inferred to be Neoproterozoic or Phanerozoic in age. Both Eury- and Crenarchaeota show increasing metabolic and physiological diversity through time. Early archaeal microbial communities were likely limited to sulfur reduction and hydrogenotrophic methanogenesis, and were confined to high-temperature geothermal environments. However, after the appearance of atmospheric oxygen, nodes containing a wide variety of traits (sulfate and thiosulfate reduction, sulfur oxidation, sulfide oxidation, aerobic respiration, nitrate reduction, mesophilic methanogenesis in sedimentary environments) appear, first in environments containing terrestrial Crenarchaeota in the Meso/Neoproterozoic followed by environments containing marine Euryarchaeota in the Neoproterozoic and Phanerozoic. This provides phylogenetic evidence for increasing complexity in the biogeochemical cycling of C, N, and S through geologic time, likely as a consequence of microbial evolution and the gradual oxygenation of various compartments within the biosphere. This work has implications not only for the large-scale evolution of microbial communities and biogeochemical processes, but also for the interpretation of microbial biosignatures in the ancient rock record.