Scleractinian corals are prolific producers of dimethylsulphoniopropionate (DMSP), but ecophysiological mechanisms influencing cellular concentrations are uncertain. While DMSP is often proposed to function as an antioxidant, interactions between specific host–symbiont genotype associations, plasticity in DMSP concentrations and environmental conditions that can either exert or alleviate oxidative stress are unclear. We used long-term (6 months) reciprocal transplantation of Stylophora pistillata hosting two distinct symbiont phylotypes along a depth gradient, clades A (<20 m) and C (>20 m), to assess the effect of change in depth (light intensity) on DMSP concentrations in relation to symbiont genotype and photoacclimation in corals between 3 and 50 m in the Gulf of Aqaba. Bathymetric distribution of total DMSP (DMSPt) per cell varied significantly while particulate DMSP (DMSPp) appeared to be unaffected by depth. Highest DMSPt concentrations in control corals occurred at 20 m. While 3-m transplants showed a significant increase in DMSPt concentration at 20 m and became affiliated with an additional genotype (C72), 50-m transplants largely persisted with their original genotype and exhibited no significant changes in DMSPt concentrations. DMSPt concentrations in transplants at both 3 and 50 m, on the other hand, increased significantly while all corals maintained their original symbiont genotypes. Photoacclimation differed significantly with transplantation direction relative to the controls. Symbionts in 3-m transplants at 20 m exhibited no changes in chlorophyll a (chl a) concentration, cell density or cell diameter while symbiont densities decreased and chl a concentrations increased significantly at 50 m. In contrast, symbiont densities in 50-m transplants remained unaffected across depths while symbiont diameters decreased. Chl a concentrations decreased at 20 m and increased at 3 m. Our results indicate that DMSPt concentrations following changes in depth are not only a function of symbiont genotype but result from different acclimation abilities of both symbiotic partners.