The success of scleractinian corals in tropical environments is mainly driven by their ability to establish symbioses with microbial partners. Yet, little is known about the eco-evolutionary forces controlling the microbial assemblage of corals. Using twelve coral species from the complex and robust clades, we carried out a detailed investigation of coral-bacterial association patterns across the skeleton and tissue of the corals. We found that the two anatomical compartments differ in microbiome composition, but a consortium of beneficial bacteria are able to colonize both, supporting the hypothesis that the skeleton can function as a reservoir. We show that host phylogeny, skeletal architecture, and reproductive mode play minor but key roles in determining the microbiome composition. Our data indicate that corals exhibit high intraspecific microbiome variability, but their association with a consortium of key bacteria is consistent across evolutionary history, with structural features and reproductive traits. The results together suggest that eco-evolutionary forces have selected a few key coral-bacterial symbioses known to aid the coral holobiont to thrive in tropical ecosystems.