Abstract The coral–dinoflagellate symbiosis is increasingly disrupted by global and local anthropogenic stressors. Coral bleaching is primarily a result of high sea surface temperatures, while eutrophication is associated with reef ecosystem degradation. Excess inorganic nitrogen relative to phosphate has been proposed to directly sensitise corals to thermal bleaching and accelerate reef decline. We assessed the proteomic response of the dinoflagellate coral symbiont Symbiodinium microadriaticum to elevated temperatures under multiple nutrient conditions by mass spectrometry. Elevated temperatures resulted in reductions of many chloroplast proteins, particularly light-harvesting complexes, with simultaneous increases in chaperone proteins. N:P imbalance had a larger effect on the proteome than temperature, but the biological processes and proteins responding to each stressor largely overlapped. The proteomes were highly similar at low N:P ratios but were strongly affected by phosphate starvation. High N:P ratios inhibited cell division, reflected by changes in proteins involved in protein translation. Imbalanced N:P did not increase sensitivity to high temperatures as measured by physiological means; however, imbalanced N:P strongly upregulated cell redox homeostasis proteins at high temperatures. As redox balance is critical during thermal bleaching, these data provide insight into the mechanisms of cellular responses to thermal and multiple stresses in the coral–dinoflagellate symbiosis.