Coral reefs are supported critically by symbioses involving dinoflagellate algae in the Family Symbiodiniaceae. Breakdown of the coral-dinoflagellate symbiosis (i.e. coral bleaching), often due to ocean warming, puts reefs at risk of starvation, disease, and eventual death. The coral symbiont Durusdinium trenchii is significant for its capacity for increasing the resilience of coral holobionts under thermal stress. Believed to have experienced whole-genome duplication (WGD), an evolutionary mechanism for functional innovation, D. trenchii offers a valuable model system to understand how selection following WGD influences the genome of a symbiont. We generated de novo genome assemblies for two isolates of D. trenchii and demonstrate whole-genome support for WGD in a eukaryotic symbiont. We assessed how the facultative lifestyle has contributed to the retention and divergence of duplicate genes (i.e. ohnologs), and how these results intersect with the observed thermotolerance of corals hosting D. trenchii symbionts. Whereas our results show the free-living lifestyle is the main driver of post-WGD evolution they also implicate symbiosis, with both lifestyles increasing fitness. We show that in an interesting and unexpected twist, WGD, driven by selection under the free-living lifestyle has converted D. trenchii into the ideal coral symbiont that is better equipped to protect the host coral from thermal stress.