The symbiosis between corals and dinoflagellate algae of the family Symbiodiniaceae is essential for the development and survival of coral reefs. Yet this fragile association is highly vulnerable to environmental disturbance. A coral’s ability to tolerate temperature stress depends on the fitness of its resident symbionts, whose thermal optima vary extensively between lineages. However, the in hospite population genetic structure of Symbiodiniaceae is poorly understood and mostly based on analysis of bulk DNA extracted from thousands to millions of cells. Using quantitative single-cell PCR, we enumerated DNA polymorphisms in the symbionts of the reef-building coral Pocillopora damicornis, and investigated the distribution of IGV Symbiodiniaceae at a variety of temporal and spatial scales. We also assessed the associations between IGV Symbiodiniaceae and coral host performance in both artificial and natural settings. We consider the evolutionary origins of prevalent IGV in Symbiodiniaceae, and its possible adaptive implications in a changing climate.