Reef-building corals form obligate symbioses with single-cell dinoflagellates of the highly diverse genus Symbiodinium. Some corals can harbour more than one Symbiodinium type in a single colony and these types may shuffle up or down in relative dominance depending on the environment. It has been hypothesized that symbiont populations may change dramatically in this manner after bleaching, if low levels of more stress-tolerant types selectively proliferate and become predominant. In this study, we investigate the genetic identity of Symbiodinium harboured by individual colonies of the reef-building coral Acropora millepora before and after a natural bleaching event in the Keppel Islands (Great Barrier Reef) using a combination of Single Strand Conformational Polymorphism (SSCP) and sequence analysis of the nuclear ribosomal Internal Transcribed Spacer 1 (ITS1) region. Before bleaching, 93.5% (n=460) of the randomly sampled and tagged colonies were dominated by Symbiodinium type C2, while the remainder harboured Symbiodinium clade D or mixtures of C2 and D. Variants of both clade D and clade C proliferated after bleaching, but the incidence of colonies predominant in clade D increased to 52% (n=79) of the tagged colonies that were re-sampled. We suggest the change in symbiont community structure occurred mainly as a result of background symbionts proliferating in recovered colonies and to a lesser extent due to selective mortality of colonies that were dominant in Symbiodinium C2 (13%, n=159). If these backgrounds symbionts are present in other structurally important coral species, coral reefs may have considerably more acclimatization potential through symbiont shuffling than previously thought.