Understanding how fish growth and reproduction will adapt to changing environmental conditions is a fundamental question in evolutionary ecology. Studies focused on the physiological effects of climate change upon life histories and population demography often ignore size-dependent foraging and risk of predation. We embedded a state-dependent energetic model in an ecosystem size spectrum to model 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 relatively small. We applied our model to scenarios corresponding to species representing the three ecological lifestyles (ecotypes) of tunas, in some cases including seasonal variation in conditions. We predicted realistic patterns of growth of tunas and found that seasonality in resource accumulation and compression of reproduction into short time periods favors growth to larger body sizes. Our framework for predicting emergent life histories combines direct and indirect effects of productivity (foodscapes), individual risk (fearscapes), and metabolic processes and offers a promising approach to understand fish life history responses to changing ocean conditions.