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Abstract The susceptibility of corals to environmental stress is determined by complex interactions between host genetic variation and the Symbiodiniaceae family community. We exposed genotypes of Montipora capitata hosting primarily Cladocopium or Durusdinium symbionts to ambient conditions and an 8-day heat stress. Symbionts’ cell surface glycan composition differed between genera and was significantly affected by temperature and oxidative stress. The metabolic profile of coral holobionts was primarily shaped by symbionts identity, but was also strongly responsive to oxidative stress. At peak temperature stress, betaine lipids in Cladocopium were remodeled to more closely resemble the abundance and saturation state of Durusdinium symbionts, which paralleled a larger metabolic shift in Cladocopium. Exploring how Symbiodiniaceae members regulate stress and host-symbiont affinity helps identify the traits contributing to coral resilience under climate change.