Massive populations of sardines inhabit both the western and eastern boundaries of the world’s subtropical ocean basins, supporting both commercial fisheries and populations of marine predators. Sardine populations in western and eastern boundary current systems have responded oppositely to decadal scale anomalies in ocean temperature, but the mechanism for differing variability has remained unclear. Here, based on otolith microstructure and high-resolution stable isotope analyses, we show that habitat temperature, early life growth rates, energy expenditure, metabolically optimal temperature, and, most importantly, the relationship between growth rate and temperature are remarkably different between the two subpopulations in the western and eastern North Pacific. Varying metabolic responses to environmental changes partly explain the contrasting growth responses. Consistent differences in the life-history traits are observed between subpopulations in the western and eastern boundary current systems around South Africa. These growth and survival characteristics can facilitate the contrasting responses of sardine populations to climate change.