In an ocean that is rapidly warming and losing oxygen, accurate forecasting of species’ responses must consider how this environmental change affects fundamental aspects of their physiology. Here, we develop an absolute metabolic index (ΦA) that quantifies how ocean temperature, dissolved oxygen and organismal mass interact to constrain the total oxygen budget an organism can use to fuel sustainable levels of aerobic metabolism. We calibrate species-specific parameters of ΦAwith physiological measurements for red abalone (Haliotis rufescens) and purple urchin (Strongylocentrotus purpuratus). ΦAmodels highlight that the temperature where oxygen supply is greatest shifts cooler when water loses oxygen or organisms grow larger, providing a mechanistic explanation for observed thermal preference patterns. Viable habitat forecasts are disproportionally deleterious for red abalone, revealing how species-specific physiologies modulate the intensity of a common climate signal, captured in the newly developed ΦAframework.