Global warming of the world's oceans is driving reef-building corals towards their upper thermal limit, inducing bleaching, nutrient starvation and mortality. In addition, corals are predicted to experience large fluctuations in seawater nutrient concentrations, following water column stratification or eutrophication problems, which can further alter their nutritional capacities and ultimately their resilience to global change. We investigated the effect of thermal stress and dissolved inorganic nutrient (DINUT) availability on the auto- and heterotrophic nutritional capacities of corals. In particular, we assessed the effect of nitrogen enrichment or DINUT depletion (both in nitrogen and in phosphorus) on the assimilation of heterotrophic nutrients and on the heat-stress tolerance of the reef-building coral Stylophora pistillata. Here, we show that DINUT depletion enhanced coral bleaching under thermal stress and more importantly, significantly impaired rates of heterotrophic nutrient assimilation, inducing coral starvation. In contrast, corals grown under nitrogen enrichment maintained high rates of heterotrophic nutrient assimilation and avoided bleaching, although nutrient uptake rates were lowered. We therefore observed a positive coupling between auto- and heterotrophy within the coral-dinoflagellate symbiosis, indicating that heterotrophic processes require a minimum of autotrophically acquired nutrients to be functional. These findings show that the trophic plasticity of corals directly depends on the availability of dissolved inorganic nutrients in seawater. The lack of a shift towards greater heterotrophy under DINUT depletion may lead to substantial modifications of the role that feeding plays in the response of reef-building corals to climate change.