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 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 duality of facultative lifestyle has contributed to the retention and divergence of duplicate genes (i.e. ohnologs) and metabolic pathways, connecting this to the observed thermotolerance of D. trenchii. While our results support the free-living lifestyle as the main driver of post-WGD evolution, they also implicate symbiosis suggesting both lifestyles drive increasing fitness. Our results show that WGD-driven selection from dual lifestyles, but primarily the free-living lifestyle, has serendipitously converted D. trenchii into an ideal coral symbiont better equipped to protect the host coral from thermal stress.