Rates of aerobic metabolism vary considerably across evolutionary lineages, but little is known about the proximate and ultimate factors that generate and maintain this variability.Using data for 131 teleost fish species, we performed a large-scale phylogenetic comparative analysis of how interspecific variation in resting and maximum metabolic rates (RMR and MMR, respectively) is related to several ecological and morphological variables. Mass-and temperature-adjusted RMR and MMR are highly correlated along a continuum spanning a 30-to 40-fold range. Phylogenetic generalized least squares models suggest RMR and MMR are higher in pelagic species and that species with higher trophic levels exhibit elevated MMR. This variation is mirrored at various levels of structural organization: gill surface area, muscle protein content, and caudal fin aspect ratio (a proxy for activity) are positively related with aerobic capacity. Muscle protein content and caudal fin aspect ratio are also positively correlated with RMR. Hypoxia-tolerant lineages fall at the lower end of the metabolic continuum. Different ecological lifestyles are associated with contrasting levels of aerobic capacity, possibly reflecting the interplay between selection for increased locomotor performance on one hand and tolerance to low resource availability, particularly oxygen, on the other. These results support the aerobic capacity model of the evolution of endothermy, suggesting elevated body temperatures evolved as correlated responses to selection for high activity levels.