Giant clams (Tridacninae) are important members of Indo-Pacific coral reefs and among the few bivalve groups that live in symbiosis with unicellular algae (Symbiodiniaceae). Despite the importance of these endosymbiotic dinoflagellates for clam ecology, the diversity and specificity of these associations remain relatively poorly studied, especially in the Red Sea. Here, we used the internal transcribed spacer 2 (ITS2) rDNA gene region to investigate Symbiodiniaceae communities associated with Red Sea Tridacna maxima clams. We sampled five sites spanning 1,300 km (10° of latitude, from the Gulf of Aqaba, 29°N, to the Farasan Banks, 18°N) along the Red Sea's North-South environmental gradient. We detected a diverse and structured assembly of host-associated algae with communities demonstrating region and site-specificity. Specimens from the Gulf of Aqaba harbored three genera of Symbiodiniaceae, Cladocopium, Durusdinium, and Symbiodinium, while at all other sites clams associated exclusively with algae from the Symbiodinium genus. Of these exclusively Symbiodinium-associating sites, the more northern (27° and 22°) and more southern sites (20° and 18°) formed two separate groupings despite site-specific algal genotypes being resolved at each site. These groupings were congruent with the genetic break seen across multiple marine taxa in the Red Sea at approximately 19°, and along with our documented site-specificity of algal communities, contrasted the panmictic distribution of the T. maxima host. As such, our findings indicate flexibility in T. maxima-Symbiodiniaceae associations that may explain its relatively high environmental plasticity and offers a mechanism for environmental niche adaptation.