Coral reefs are among the most biodiverse ecosystems on Earth and rely on endosymbiosis with Symbiodiniaceae, a diverse family of dinoflagellates essential for coral nutrition and which also play an important role in thermal tolerance. Despite their ecological importance, resolving species boundaries within Symbiodiniaceae remains challenging, partly due to limited phylogenetic signal in commonly used genetic markers and the absence of broadly accepted criteria for species delimitation. Refining taxonomic resolution is therefore critical for understanding symbiont diversity, distributions, and evolutionary relationships. In this study, we delimit two closely related Cladocopium species using a meta-haplotype framework applied to two hypervariable loci—the ITS2 region and the psbA non-coding region (psbAncr). Slowly evolving markers fail to differentiate Cladocopium proximale (SCF049; described here) and its sister species C. proliferum, yet consistent and biologically meaningful variation is captured across both hypervariable regions. By integrating divergence across multiple organellar and nuclear regions, we demonstrate that C. proximale and C. proliferum represent distinct species. More broadly, closely related Symbiodiniaceae such as these provide important systems for examining speciation processes, including potential ecological differentiation and reproductive compatibility. Our results highlight the value of combining multiple hypervariable markers to improve taxonomic accuracy in Symbiodiniaceae and strengthen the basis for identifying and describing closely related species within this ecologically crucial group.