There is currently much debate about the ecological advantages for reef corals of hosting multiple types of the symbiotic dinoflagellate Symbiodinium. Amongst these is their apparent capacity to tolerate higher than normal water temperatures. There is strong photokinetic evidence that the trait of heat-tolerance in plants is accompanied by energetic tradeoffs but little such evidence yet exists for corals. We use rapid light curves (RLCs) to investigate the photokinetic basis for thermo-tolerance in the reef coral Acropora millepora with symbionts of contrasting thermal tolerance for which there are measured differences in energetics. Our results show that under non-stressful temperatures, corals with heat-tolerant type D Symbiodinium had a 41% lower maximum relative electron transport rate (rETRmax) and lower light absorption efficiency (α) due to lower cell Chl a content compared with corals with heat-sensitive type C2 symbionts. Our results provide support for a photokinetic link between heat tolerance and deficits in holobiont (coral + symbiont) growth, lipid stores and reproduction. Reduced electron transport rate and light absorption capacity may be genotype-specific attributes that enable clade D symbionts and their cnidarian hosts to cope with temperature stress but they inherently influence the photosynthetic function of the symbionts and thus have negative downstream effects on the coral.