Updated project metadata. The Placozoa are an enigmatic group of simple marine metazoans where all taxa harbor intracellular bacteria. Despite four decades of research, the bacterial identities, their location and their roles remain elusive. Here we show that the placozoan Trichoplax H2 is associated with two intracellular bacteria. We detected the symbionts and reconstructed their physiology using metagenomic and metatranscriptomic evidence from the same single-animal specimens. One symbiont forms a new genus in the Midichloriaceae (Rickettsiales) and correlative fluorescent labelling and 3-D electron microscopic tomography showed that it inhabits the rough ER in the fiber-cells. It has mutualistic traits and occurs worldwide as we could detect it in 10% of all aquatic tag sequencing datasets. The second symbiont is an intracellular bacterium from the Margulisbacteria, a phylum-level clade previously only identified from DNA sequencing and not known to form intracellular associations. It resides in the digestive ventral epithelial cells, uses lipids digested by the host and has the physiological capacity to supplement the placozoan nutrition. Our single-individual approach revealed that this cultivable placozoan host forms a tripartite symbiosis and provides experimental access to microbial dark matter – a rickettsiales that inhabits a novel niche within eukaryote cells and an intracellular margulisbacterial symbiont.