Coral bleaching is primarily caused by high sea surface temperatures, and nutrient enrichment of reefs is associated with lower resilience to thermal stress and ecological degradation. Excess inorganic nitrogen relative to phosphate has been proposed to sensitise corals to thermal bleaching. We assessed the physiological and proteomic responses of cultures of the dinoflagellate coral symbiont Symbiodinium microadriaticum to elevated temperature under low-nutrient, high-nutrient, and phosphate-limited conditions. Elevated temperature induced reductions of many chloroplast proteins, particularly the light-harvesting complexes, and simultaneously increased the abundance of many chaperone proteins. Proteomes were similar when the N:P ratio was near the Redfield ratio, regardless of absolute N and P concentrations, but were strongly affected by phosphate limitation. Very high N:P inhibited Symbiodinium cell division while increasing the abundances of chloroplast proteins. The proteome response to phosphate limitation was greater than that to elevated temperature, as measured by the number of differentially abundant proteins. Increased physiological sensitivity to high temperatures under high nutrients or imbalanced N:P was not apparent; however, oxidative stress response proteins were enriched amongst proteins responding to thermal stress under imbalanced N:P ratios. These data provide a detailed catalogue of the effects of high temperatures and nutrients on a coral symbiont proteome.