<p>Coral bleaching is one of the greatest threats to the persistence of tropical reef ecosystems. This necessitates identification of attributes associated with coral resistance and resilience to thermal stress, both within and between generations. Here, we use metabolomics to investigate the intergenerational biochemical signatures associated with heat-induced bleaching of <i>Montipora capitata</i> (the rice coral). By selectively breeding bleaching resistant or susceptible parents, we find metabolomic signatures of parental bleaching phenotype in sperm, eggs, embryos, larvae, and subsequent juvenile corals. Metabolome source mapping shows that these thermal tolerance signatures are from both coral host and algal symbiont, spanning a variety of molecular families. One of the strongest markers of intergenerational heat tolerance is the saturation state of DGCC betaine lipids, a molecular family previously associated with thermal tolerance in dinoflagellate symbionts of corals. Though DGCC lipid saturation state is strongly linked to algal genotypes, even coral progeny containing the more thermally susceptible <i>Cladocopium</i> algae show increased saturation of this lipid group if their parents had resisted recent bleaching events. This work provides evidence for biochemical inheritance as a potential mechanism for intergenerational acclimatization to warming oceans, which has substantial implications for reef conservation and restoration in the face of climate change.</p>