Sea surface temperatures (SST) and chlorophyll a concentrations (Chl a) in the southern Red Sea have wide variations based on distance from the coast. To understand how these variations can affect the diversity of symbionts hosted by reef-associated organisms, we conducted a study in the central and southern Red Sea to examine the diversity of Symbiodiniaceae hosted by the zooxanthellate zoantharian Palythoa tuberculosa at different distances from the coast: offshore (FBO), midshelf (FBM) and inshore (FBI) of Farasan Banks, and inshore at Thuwal (TI). Genomic DNA was extracted from 198 specimens, followed by amplification of the ribosomal DNA internal transcribed spacer 2 (ITS-2) and noncoding region of the chloroplast plastid minicircle (psbAncr). Durusdinium and six lineages of Cladocopium (Pt-1-a, Pt-1-b, Pt-1-c, Pt-1-d, Pt-3-a, Pt-3-b) were identified based on sequences of the two marker regions. Changes in composition of Symbiodiniaceae lineages were observed from FBI (high SST, high Chl a) to FBO (low SST, low Chl a). Molecular variance analyses showed that distance from coast was the most likely predictor of differences in Cladocopium lineages. Multinomial logistic regression analysis showed a transition among different Cladocopium lineages as SST increased. One Cladocopium lineage, Pt-1-b, demonstrated higher prevalences at high SSTs and increased in prevalences at the same rate as thermotolerant Durusdinium. Additionally, Cladocopium lineage Pt-3-a had a high affinity to low Chl a concentrations. This study demonstrates that environmental variations in SSTs and Chl a concentrations are significant predictors for the diversity of dominant Symbiodiniaceae within individual host P. tuberculosa colonies. We theorize that flexibility with different lineages of Symbiodiniaceae allows generalist P. tuberculosa to live across a wide range of environments in the southern Red Sea.