To persist in oligotrophic waters, reef-building corals rely on nutritional interactions with symbiotic dinoflagellates of the family Symbiodiniaceae, but the true diversity of this family remains poorly characterised. In this paper, we assess Symbiodiniaceae richness at Atauro Island (Timor-Leste) as well as on reefs of the neighbouring Timor mainland, using direct sequencing of three gene regions: cob gene, mitochondrion; ITS2 region, nucleus; and psbA ncr region, chloroplast; in addition to a highly multiplexed application of next-generation sequencing. These geographic sites are among the most biodiverse in the world, but have never had their symbiont communities studied. Despite their proximity, our results reveal symbiont richness 1.25 times higher at Atauro Island than the Timor mainland, a result evident in dominant sequences. In contrast, Timor had a significantly richer background sequence diversity. Although sampling was restricted to shallow sites only, symbiont richness at Atauro Island was also higher than comparative reefscapes globally, after standardising for number of taxa sampled. While Atauro and Timor have related symbiont populations, with the same novel types recorded at both sites, there were also clear differences in symbiont composition between the two geographic regions, with Timor displaying a consortium more characteristic of stressed reef environments (proportionally hosting twice as many Durusdinium sequences, formerly clade D, as Atauro). These results reveal a symbiont richness that matches the high biodiversity of these reefs, but also potentially negative effects of proximal human populations on Symbiodiniaceae, even when previous studies have shown corals to be largely unaffected.