We dissect the primary photo-inactivation and the counteracting metabolic repair rates in fragments of the scleractinian coral, Pocillopora damicornis, subjected to a combined stress of a shift to elevated temperature (from 26°C to 32°C) and increased light (from 200 μmol photons m-2 s-1 to 400 μmol photons m-2 s-1) to induce bleaching. During the bleaching treatment the dinoflagellate symbionts showed a 5.5-fold acceleration in their photosystem II (PSII) repair rate constant, demonstrating that they maintain strong metabolic capacity to clear and replace photo-damaged D1 protein at the elevated temperature and light conditions. Nevertheless, the symbionts concurrently suffered a seven-fold increase in the rate constant for PSII photo-inactivation. This rapid photo-inactivation exceeded the PSII repair capacity, therefore tipping the symbionts, and by implication the symbiosis, into net photo-inhibition. Increased photo-inactivation in hospite, rather than an inhibition of PSII repair, is the principle trigger for net photo-inhibition under bleaching conditions.