The migration and dispersal of stress-tolerant symbiotic dinoflagellates (genus Symbiodinium) may influence the response of symbiotic reef-building corals to a warming climate. We analyzed the genetic structure of the stress-tolerant endosymbiont, Symbiodinium glynni nomen nudum (ITS2 - D1), obtained from Pocillopora colonies that dominate eastern Pacific coral communities. Eleven microsatellite loci identified genotypically diverse populations with minimal genetic subdivision throughout the Eastern Tropical Pacific, encompassing 1000's of square kilometers from mainland Mexico to the Galapagos Islands. The lack of population differentiation over these distances corresponds with extensive regional host connectivity and indicates that Pocillopora larvae, which maternally inherit their symbionts, aid in the dispersal of this symbiont. In contrast to its host, however, subtropical populations of S. glynni in the Gulf of California (Sea of Cortez) were strongly differentiated from populations in tropical eastern Pacific. Selection pressures related to large seasonal fluctuations in temperature and irradiance likely explain this abrupt genetic discontinuity. We infer that S. glynni genotypes harbored by host larvae arriving from more southern locations are rapidly replaced by genotypes adapted to more temperate environments. The strong population structure of S. glynni corresponds with fluctuating environmental conditions and suggests that these genetically diverse populations have the potential to evolve rapidly to changing environments and reveals the importance of environmental extremes in driving microbial eukaryote (e.g., plankton) speciation in marine ecosystems.