Temperature is a key variable in biological processes. However, a complete understanding of biological temperature adaptation is lacking, in part because of the unique constraints among different evolutionary lineages and physiological groups. Here we compared the genomes of cultivated psychrotolerant and thermotolerant methanogens, which are physiologically related and span growth temperatures from -2.5 °C to 122 °C. Despite being phylogenetically distributed amongst three phyla in the archaea, the methanogenic genome core comprises about one third of a given methanogen’s genome, and the genome fraction shared by any two organisms decreases with increasing phylogenetic distance between them. Increased growth temperature is associated with reduced genome size, and thermotolerant organisms have larger core genome fractions, suggesting that genome reduction is governed by temperature rather than phylogeny. Thermotolerant methanogens are enriched in metal and other transporters, and psychrotolerant methanogens are enriched in proteins related to structure and motility. Observed amino acid compositional differences between temperature groups include proteome charge, polarity, and unfolding entropy. Our results suggest that in the methanogens, shared physiology maintains a large, conserved core even across large phylogenetic distances and biology’s temperature extremes.