Understanding how changing environmental conditions affect fish growth and reproduction is critical to predict the consequences of climate change, yet studies focused on the physiological effects of temperature upon life histories often ignore size-dependent foraging and risk of predation. We embedded a state-dependent energetic model in an ecosystem size spectrum model to characterize prey availability (foraging) and risk of predation (fear) experienced by individual fish as they grow. We examined how spectrum richness and temperature interact to shape growth, reproduction, and survival; we found that richer spectra led to larger body sizes, but effects of temperature on body size were small. We applied our model to scenarios corresponding to three ecological lifestyles (ecotypes) of tunas, in some cases including seasonal variation in conditions. We predicted realistic estimates of growth and body sizes of tunas and found that seasonality in resources and temperature could lead to giant body sizes (> 300 cm), due to the compression of reproduction into shorter timeframes. Our framework for predicting emergent life histories combines direct and indirect effects of productivity (foodscapes), individual risk (fearscapes), and metabolic processes. This approach can be used to reconcile disparate results on fish life history responses to changing ocean conditions.