Extremophiles survive in environments that are considered uninhabitable for most living things. The evolution of extremophiles is of great interest because of how they may have contributed to the assembly of ecosystems, yet the evolutionary dynamics that drive extremophile evolution remain obscure. Here, we investigate the evolution of extremophiles in , a lineage of over 300 species of fishes that have colonized both poles, the deep sea, and hydrothermal vents. We show that a pulse of habitat invasion occurred across over 20 different zoarcoid lineages within the last 8 million years, far after the origin of their prototypical innovation for surviving in cold water: type III antifreeze protein. Instead, a secondary burst of anatomical, physiological and life history traits and a handful of founder events in extreme ecosystems appear to have propelled zoarcoid diversification. These results decentralize the role of prototypical changes to organismal biology in shaping extremophile radiations and provide a clear example of how a combination of ancient adaptations and recent contingency shapes the origination of lineages in challenging habitats.