On coral reefs, some of the most aggressive calcium carbonate eroders are dinoflagellate-hosting sponges of the genus Cliona. Like in other marine taxa, the influence of these symbiotic microorganisms on the metabolism of the host sponge, and thereby on erosion of the surrounding ecosystem, is increasingly acknowledged. Despite elevating pH (and hence carbonate saturation state), dinoflagellate photosynthesis promotes bioerosion by their hosts. This paradox might be solved by a spatial isolation of photosynthesis from carbonate dissolution, but it remains unknown which mechanism connects the dinoflagellates’ photosynthesis with the sponge’s bioerosion. Here, we simulate the outcomes of photosynthesis in two separate ways, namely as production of carbon-rich compounds (in this case glycerol) and as an increase in oxygen content. This allows testing their potential to enhance bioerosion rates of sponge holobionts that were preconditioned under variable photosynthetic regimes. We find that glycerol, a commonly shared photosynthate in marine symbioses, stimulates chemical bioerosion rates in the dark of photosynthetically impaired sponges. Chemical bioerosion was all the more limited by availability of sufficient oxygen, while the combination of added glycerol and oxygen boosted chemical bioerosion rates. We argue that under normal physiological conditions, bioerosion is promoted by both organic carbon and oxygen production, and we provide evidence for the storage of photosynthates for night-time use. We further discuss our findings in the context of the current knowledge of the bioerosion mechanism, which we expand by integrating the effects of carbon-rich compounds and oxygen as drivers for bioerosion by Cliona.