Studying carbon dynamics in the coral holobiont provides essential knowledge of nutritional strategies and is thus central to understanding coral ecophysiology. In this study, we assessed the carbon budget in Pocillopora damicornis (usingH13CO3) as a function of feeding status and temperature stress. We also compared dissolved oxygen (O2) fluxes measured at the colony scale and at the polyp scale. At both scales, O2 production rates were enhanced for fed vs. unfed corals, and unfed corals exhibited higher bleaching and reduced photosynthetic activity at high temperature. Unfed corals exclusively respired autotrophically acquired carbon, while fed corals mostly respired heterotrophically acquired carbon. As a consequence, fed corals excreted on average >5 times more organic carbon than unfed corals. Photosynthate translocation was higher under thermal stress, but most of the carbon was lost via respiration and/or mucus release (42−46% and 57−75% of the fixed carbon for unfed and fed corals, respectively). Such high loss of translocated carbon, coupled to low assimilation rates in the coral tissue and symbionts, suggests that P. dami - cornis was nitrogen and/or phosphorus limited. Heterotrophy might thus cover a larger portion of the nutritional demand for P. damicornis than previously assumed. Our results suggest that active feeding plays a fundamental role in metabolic dynamics and bleaching susceptibility of corals.