The increasing severity and frequency of mass bleaching events has placed shallow-water tropical coral reefs at risk of significant decline in the coming decades. The association of endosymbiotic dinoflagellates (Family: Symbiodiniaceae) with corals is regulated by local environmental conditions along with evolutionary history and plays a leading role in bleaching sensitivity and recovery. Resolving temporal and spatial dynamics of coral-Symbiodiniaceae associations is therefore essential for accurate bleaching risk predictions. Here, we investigated temporal patterns in dominant Symbiodiniaceae across the Greater Caribbean region, which is heavily impacted by human activities, disease and climate change. Using records derived from genetic databases, we considered Symbiodiniaceae dominance from 1994 to 2009, with a particular focus on and around the 2005 mass bleaching event. From the 4 Symbiodiniaceae genera recorded ( Symbiodinium , Breviolum , Cladocopium and Durusdinium spp.), we identified genera-specific responses to ocean heating and bleaching stress. Generalist symbiont representatives were dominant only during periods of sustained environmental stability. In contrast, during and immediately after bleaching saw the emergence and subsequent persistence of Durusdinium spp.—an invasive genus in the Caribbean with high thermal tolerance but which induces negative impacts on coral physiology and calcification. In post-bleaching recovery years, a regional-scale bet-hedging strategy was adopted allowing thermal tolerance to be maintained, but poised for a more physiologically beneficial symbiosis if/when environmental conditions become favourable. Our regional-scale, multi-year perspective gives support for local-/colony-scale tuning of coral-Symbiodiniaceae relationships, and highlights how continued warming and bleaching stress will enable Durusdinium spp. invasion to persist, with knock-on implications for future coral reef development.