The origins of endothermy in birds and mammals are important events in vertebrate evolution. Endotherms can maintain their body temperature (T b ) over a wide range of ambient temperatures primarily using the heat that is generated continuously by their high basal metabolic rate (BMR)1. There is also an important positive feedback loop as T b influences BMR1,2,3. Owing to this interplay between BMRs and T b , many ecologists and evolutionary physiologists posit that the evolution of BMR and T b must have been coupled during the radiation of endotherms3,4,5, changing with similar trends6,7,8. However, colder historical environments might have imposed strong selective pressures on BMR to compensate for increased rates of heat loss and to keep T b constant9,10,11,12. Thus, adaptation to cold ambient temperatures through increases in BMR could have decoupled BMR from T b and caused different evolutionary routes to the modern diversity in these traits. Here we show that BMR and T b were decoupled in approximately 90% of mammalian phylogenetic branches and 36% of avian phylogenetic branches. Mammalian BMRs evolved with rapid bursts but without a long-term directional trend, whereas T b evolved mostly at a constant rate and towards colder bodies from a warmer-bodied common ancestor. Avian BMRs evolved predominantly at a constant rate and without a long-term directional trend, whereas T b evolved with much greater rate heterogeneity and with adaptive evolution towards colder bodies. Furthermore, rapid shifts that lead to both increases and decreases in BMRs were linked to abrupt changes towards colder ambient temperatures—although only in mammals. Our results suggest that natural selection effectively exploited the diversity in mammalian BMRs under diverse, often-adverse historical thermal environments.