Partner-switching plays an important role in the evolution of symbiosis, enabling local adaptation and recovery from the breakdown of symbiosis. Because of intergenomic epistasis, partner-switched symbioses may possess novel combinations of phenotypes but may also exhibit low fitness due to their lack of recent coevolutionary history. Here, we examine the structure and mechanisms of intergenomic epistasis in the Paramecium-Chlorella symbiosis and test if compensatory evolution can rescue initially low fitness partner-switched symbioses. Using partner-switch experiments coupled with metabolomics we show evidence for intergenomic epistasis wherein low fitness arose from mismatched photoprotection traits and the resulting light stress experienced by non-native symbionts when in high light environments. Experimental evolution under high light conditions revealed that an initially low fitness partner-switched non-native host-symbiont pairing rapidly adapted, gaining fitness equivalent to the native host symbiont pairing in less than 50 host generations. Compensatory evolution took two alternative routes: Either, hosts evolved higher symbiont loads to mitigate for their new algal symbiont's poor performance, or the algal symbionts themselves evolved higher investment in photosynthesis and photoprotective traits to better mitigate light stress. These findings suggest that partner-switching combined with rapid compensatory evolution will enable the recovery and local adaptation of symbioses in response to changing environments.