Corals are associated with a variety of bacteria, which occur in the surface mucus layer, gastrovascular cavity, skeleton, and tissues. Some tissue-associated bacteria form clusters, termed cell-associated microbial aggregates (CAMAs), which are poorly studied. Here, we provide a comprehensive characterization of CAMAs in the coral Pocillopora acuta. Combining imaging techniques, laser capture microdissection, and amplicon and metagenome sequencing we show that CAMAs: (i) are located in the tentacle tips and may be intracellular; (ii) contain Endozoicomonas, Kistimonas (both Gammaproteobacteria), and Simkania (Chlamydiota) bacteria; (iii) Endozoicomonas may provide vitamins to its host and use secretion systems and/or pili for colonization and aggregation; (iv) Endozoicomonas and Simkania occur in distinct, but adjacent, CAMAs; (v) Simkania may rely on acetate and heme provided by neighboring Endozoicomonas. Our study provides detailed insight into coral endosymbionts, which will guide the assessment of their suitability for probiotic approaches to mitigate coral bleaching.