Reef corals are sentinels for the adverse effects of rapid global warming on the planet's ecosystems. Warming sea surface temperatures have led to frequent episodes of bleaching and mortality among corals that depend on endosymbiotic micro-algae (Symbiodinium) for their survival. However, our understanding of the ecological and evolutionary response of corals to episodes of thermal stress remains inadequate. For the first time, we describe how the symbioses of major reef-building species in the Caribbean respond to severe thermal stress before, during and after a severe bleaching event. Evidence suggests that background populations of Symbiodinium trenchi (D1a) increased in prevalence and abundance, especially among corals that exhibited high sensitivity to stress. Contrary to previous hypotheses, which posit that a change in symbiont occurs subsequent to bleaching, S. trenchi increased in the weeks leading up to and during the bleaching episode and disproportionately dominated colonies that did not bleach. During the bleaching event, approximately 20 per cent of colonies surveyed harboured this symbiont at high densities (calculated at less than 1.0% only months before bleaching began). However, competitive displacement by homologous symbionts significantly reduced S. trenchi's prevalence and dominance among colonies after a 2-year period following the bleaching event. While the extended duration of thermal stress in 2005 provided an ecological opportunity for a rare host-generalist symbiont, it remains unclear to what extent the rise and fall of S. trenchi was of ecological benefit or whether its increased prevalence was an indicator of weakening coral health.