Climate-ready fisheries management requires reliable predictions of species responses to changing conditions across large-scale environmental gradients. Bioenergetic frameworks, such as Dynamic Energy Budget (DEB) models, relate physiological processes to environmental conditions, enabling predictions of organismal growth under projected climate change conditions. Here, we provide the first large-scale coupling of a DEB model to downscaled regional oceanographic simulations to resolve spatiotemporal changes and reveal how climate stressors emerge at relevant biogeographic, economic, and oceanographic scales. We calibrated our DEB model for the Atlantic sea scallop (Placopecten magellanicus) with forcing from a realistic oceanographic and biogeochemical model for the Northeast U.S. continental shelf to predict the effects of ocean acidification (OA) and warming on individual growth historically and over the next century. Our model reproduced observed historical patterns in scallop age at harvest size and maximum size. At mid-century (2035–2050), scallop growth was projected to increase in most areas except the southern Mid-Atlantic, and OA effects were limited to the deep Gulf of Maine. By the end of the century (2080–2095) under a high emissions scenario, scallops were predicted to grow faster but attain smaller maximum sizes. Our results highlight that warming stress is more acute than previously accounted for, particularly in the southern Mid-Atlantic. While warming stress emerges in the south first, OA stress emerges before warming in the north. Together, these emerging stressors compress the spatial range for optimal growth. Altogether, our findings demonstrate the utility of the spatially coupled DEB model as a tool to inform adaptive fisheries management.