The symbiosis between dinoflagellate microalgae and their cnidarian host represents the fundamental mechanism that allows zooxanthellate corals to access the inorganic nutrient pool of the surrounding seawater and conserve and recycle nutrients within their tissues. Experiments have shown that colony symbiont density is strongly affected by ambient nitrogen levels and the nitrogen status of the host. Under oligotrophic conditions, the symbiont population is N- and potentially DIC-limited. Here, we investigated how a feeding-induced increase in colony symbiont density modulates the phototrophic assimilation of individual symbionts. Using stable isotopes in combination with NanoSIMS-imaging of fixed coral coenosarc tissue, we quantified in hospite C and N assimilation of individual symbionts and related these values to the local tissue density. Stylophora pistillata displayed a general negative correlation between colony symbiont density and symbiont carbohydrate and protein content, independent of feeding state. Under unfed conditions, cell-specific assimilation rates for C and N were not affected by local symbiont density. However, when the colony symbiont density was increased by regular feeding, we observed a significant negative effect: Individual autotrophic assimilation of C and N declined on average by 26% for a local density range from one to ten Symbiodinium cells. Thus, the increase in global symbiont density created conditions where symbionts in some microhabitats might be subject to competition, governed by individual performance, local host supply or light microenvironment.