Thermal tolerance is often used to explain range limits, abundance, and population dynamics; however, recent theory suggests thermal tolerance itself can be fundamentally altered by food limitation. We tested this hypothesis by quantifying how temperature and food concentrations interact synergistically to shape growth, development, and survival throughout larval development of purple urchins (Strongylocentrotus purpuratus). Developmental rates and time to metamorphic competency were driven largely by temperature but were not affected by the range of food concentrations. However, food limitation had a substantial impact on survival response to temperature. With ample food, larvae exhibited modest survival across temperatures currently experienced by larvae in nature. Reductions in food lowered optimal survival temperatures and shifted the thermal window towards cooler temperatures. These results are consistent with the “metabolic meltdown” hypothesis - shifting optima to cooler temperatures- and illustrate how present day warming with lower productivity may lead to substantial, unexpected declines in larval recruitment.