Endozoicomonas bacteria are emerging as extremely diverse and flexible symbionts of numerous marine hosts inhabiting oceans worldwide. Their hosts range from simple invertebrate species, such as sponges and corals, to complex vertebrates, such as fish. Although widely distributed, the functional role of Endozoicomonas within their host microenvironment is not well understood. Using corals as a model to understand spatial and host taxonomic specificity, we show that distinct Endozoicomonas taxa reside deep within host tissues and their diversity is linked to host reproductive strategy. Further, we generated novel Endozoicomonas genomes from single cells and metagenomes obtained directly from coral hosts, and compared these to existing genomes of bacterial isolates acquired from a sponge, sea slug, and coral to examine the functional landscape of this enigmatic genus. Genomic analyses suggest that Endozoicomonas have a free-living stage due to their large genome sizes, show signs of host and local adaptation, participate in host-associated protein and carbohydrate transport and cycling, and harbor a high degree of genomic plasticity due to the large proportion of transposable elements residing in their genomes. Given this diversity of Endozoicomonas we propose that different genotypes play disparate roles and have evolved in concert with their diverse hosts.