The ecological success of many invertebrates relies on their metabolic exchanges with symbionts. In coral reef ecosystems, ocean warming can destabilize host-symbiont dynamics, leading to the breakdown of the symbiosis. In contrast to most coral species, sponge-Symbiodiniaceae associations show high resistance to increasing temperatures, though the molecular pathways contributing to this response are still unknown. Here, we characterized the molecular mechanisms underpinning host-symbiont interactions under prolonged heat stress in the sponge Cliona orientalis and the coral Porites lutea through a 2-month experiment using physiological metrics and omics-based tools (transcriptomics and 16S rRNA gene sequencing). While Symbiodiniaceae gene expression patterns were similar within both holobiont hosts, host transcriptomic responses to moderate heat stress (3 Degree Heating Weeks) differed markedly between the two species. In the coral holobiont, the destabilisation of symbiosis under heat stress was associated with a decoupling of carbon recycling and an increase in nitrogen availability. Whilst carbon metabolism was also altered within the sponge holobiont, no strong changes to nitrogen cycling were observed. Additionally, physiological stress signatures were coupled with a shift in the microbial community only in the coral holobiont. Our findings suggest differences in nutrient recycling may underpin the stability of reef symbioses under heat stress.