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Abstract Alterations of marine species’ ranges with climate change are often attributed to oxygen limitation in warming oceans. Here we report unique metabolic temperature sensitivities for the myriad of vertically migrating oceanic species that daily cross depth-related gradients in temperature and oxygen. In these taxa, selection favours high metabolic activity for predator–prey interactions in warm shallow water and hypoxia tolerance in the cold at depth. These diverging selective pressures result in thermal insensitivity of oxygen supply capacity and enhanced thermal sensitivity of active metabolic rate. Aerobic scope is diminished in the cold, well beyond thermodynamic influences and regardless of ambient oxygen levels, explaining the native distributions of tropical migrators and their recent range expansions following warming events. Cold waters currently constitute an energetic barrier to latitudinal range expansion in vertical migrators. As warming due to climate change approaches, and eventually surpasses, temperatures seen during past warming events, this energetic barrier will be relieved.