AbstractThe existence of widespread species with the capacity to endure diverse, or variable, environments are of importance to ecological and genetic research, and conservation. Such “ecological generalists” are more likely to have key adaptations that allow them to better tolerate the physiological challenges of rapid climate change. Reef‐building corals are dependent on endosymbiotic dinoflagellates (Family: Symbiodiniaceae) for their survival and growth. While these symbionts are biologically diverse, certain genetic types appear to have broad geographic distributions and are mutualistic with various host species from multiple genera and families in the order Scleractinia that must acquire their symbionts through horizontal transmission. Despite the considerable ecological importance of putative host‐generalist symbionts, they lack formal species descriptions. In this study, we used molecular, ecological, and morphological evidence to verify the existence of five new host‐generalist species in the symbiodiniacean genus Cladocopium. Their geographic distribution and prevalence among host communities corresponds to prevailing environmental conditions at both regional and local scales. The influence that each species has on host physiology may partially explain regional differences in thermal sensitivities among coral communities. The potential increased prevalence of a generalist species that endures environmental instability is a consequential ecological response to warming oceans. Large‐scale shifts in symbiont dominance could ensure reef coral persistence and productivity in the near term. Ultimately, these formal designations should advance scientific communication and generate informed research questions on the physiology and ecology of coral‐dinoflagellate mutualisms.