Relationships between animals and their associated microbiota are dependent on both the evolutionary history of the host and on the environment. The majority of studies tend to focus on either one of these factors but rarely consider how both determine the community composition of the associated microbiota. One 'natural experiment' to test how evolutionary history, shared environments, and the interaction between these factors drive community composition is to compare geminate species pairs. Echinoids separated by the Isthmus of Panama are suitable for this comparison due to their known evolutionary history and differences in the oceanographic characteristics of the Caribbean Sea and the Pacific Ocean. By comparing the bacterial communities of the eggs of Echinometra and Diadema geminate species pairs, we show that each pair of geminate species associates with a distinct bacterial community in a pattern consistent with phylosymbiosis, and that the interaction between the evolutionary history of the host and the environment best explains differences in these communities. Moreover, we found that the relative abundance of particular bacterial taxa differed considerably between the 2 bodies of water and that the 2 Caribbean Echinometra species were dominated by unclassified bacterial taxa within the phototrophic Oxyphotobacteria . Taken together, data presented here support the hypothesis that the bacterial communities associated with geminate species are another characteristic of these species that have diverged in ~2.8 million years of isolation.