Climate warming causes coral bleaching, the loss of symbiotic microalgae (Symbiodiniaceae) from coral tissues. Introducing thermally resilient Symbiodiniaceae into corals may enhance coral bleaching tolerance. Using menthol bleaching on adult Galaxea fascicularis, we removed ~99% of the coral’s native Symbiodiniaceae and inoculated them with wild-type (WT) or experimentally evolved, heat-tolerant (SS) Symbiodiniaceae (Cladocopium C1acro) under ambient conditions. Eighteen weeks after the first inoculation, WT and SS Symbiodiniaceae accounted for ~84 % and ~62 % of the coral’s Symbiodiniaceae community, respectively. Subsequent exposure to 31.5°C showed corals with the SS strain had better survival, growth and photochemical efficiency than those with WT. The proportion of SS Symbiodiniaceae in corals remained unchanged after 8 days at elevated temperature, but the abundance of the WT strain decreased by ~20% relative to the native symbiont. To explore the nutrient exchange dynamics between the corals, SS and WT Symbiodiniaceae, we pioneered a spatial metabolomics method using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI), and revealed the distributions of metabolites, lipids, and peptides in coral sections at 50 µm resolution. Our findings demonstrate experimental evolution of Symbiodiniaceae can boost thermal bleaching tolerance of adult corals, and provide deeper understanding of the mechanisms underpinning this enhanced tolerance.