Dinoflagellates of the genus Symbiodinium are symbiotic with a wide range of marine invertebrates. Broadly described as a mutualistic symbiosis, possible parasitic tendencies of Symbiodinium are less well known. The present study investigated the potential for mutualistic Symbiodinium to become parasitic in the excavating sponge Cliona orientalis, a ubiquitous bioeroder on Indo-Pacific coral reefs. We report the surprising observation that the growth, asexual reproduction and population density of Symbiodinium in C. orientalis were apparently unaffected when photosynthesis was reduced to zero in complete darkness for 20 days. Symbiodinium remained functional in hospite following the dark treatment, although with reduced photosynthetic efficiency compared to the control treatment under a daily light cycle. Rates of dark respiration and net uptake of heterotrophic carbon by the holobiont were similar between the control and dark treatments. However, dark-treated C. orientalis displayed a negative carbon budget that indicated compromised host growth, along with reduced biomass and bioerosion capability. Our findings suggest that, when lacking photo-autotrophic energy, Symbiodinium possibly sustains itself through heterotrophy at the expense of its hosts. This transfer of host materials to the symbiont suggests parasitism that may be associated with the observed deterioration of C. orientalis in the dark treatment. Overall, our study implies plasticity of Symbiodinium in terms of shifting its symbiotic role between mutualism and parasitism.