Reef-building corals are fundamental to the most diverse marine ecosystems, yet a detailed understanding of the processes involved in the establishment, persistence and ecology of the coral–dinoflagellate association remains largely unknown. This study explores symbiont diversity in relation to habitat by employing a broad-scale sampling regime using ITS2 and denaturing gradient gel electrophoresis. Samples from Pocillopora damicornis, Stylophora pistillata and Seriatopora hystrix all harboured host-specific clade C symbiont types at Heron Island (Great Barrier Reef, Australia). While Ser. hystrix associated with a single symbiont profile along its entire depth distribution, both P. damicornis and Sty. pistillata associated with multiple symbiont profiles that showed a strong zonation with depth. It is shown that, with an increased sampling effort, previously identified ‘rare’ symbiont types within this group of host species are in fact environmental specialists. A multivariate approach was used to expand on the common distinction of symbionts by a single genetic identity. It shows merit in its capacity not only to include all the variability present within the marker region but also to reliably represent ecological diversification of symbionts. Furthermore, the cohesive species concept is explored to explain how niche partitioning may drive diversification of closely related symbiont lineages. This study provides thus evidence that closely related symbionts are ecologically distinct and fulfil their own niche within the ecosystem provided by the host and external environment.