Birds, mammals, and certain fishes, including tunas, opahs and lamnid sharks, are endothermic, conserving internally generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas, among the most threatened, but commercially important, fishes worldwide are renowned regional endotherms, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tuna, such as yellowfin, by contrast, remain in warm-temperate to tropical waters year-round, reproducing more rapidly than temperate bluefin tuna. Thereby, they are more resilient to fisheries, whereas bluefins have declined steeply. Despite the importance of these traits to not only fisheries, but response to climate change, little is known of the genetic processes underlying the diversification of tuna. In collecting and analysing sequence data across 29,556 genes, we found that parallel selection on standing genetic variation has driven the evolution of endothermy in bluefin tunas. This includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme which underlies thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, β-oxidation and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two species. Phylogeny-based metrics highlight conservation needs for some of these species.