Microbes perform critical functions in corals, yet most knowledge is derived from the photic zone. Here, we discover two mollicutes that dominate the microbiome of the deep-sea octocoral, Callogorgia delta, and likely reside in the mesoglea. These symbionts are abundant across the host’s range, absent in the water, and appear to be rare in sediments. Unlike other mollicutes, they lack all known fermentative capabilities, including glycolysis, and can only generate energy from arginine provided by the coral host. Their genomes feature several mechanisms to interact with foreign DNA, including extensive CRISPR arrays and restriction-modification systems, which may indicate their role in symbiosis. We propose the novel family Oceanoplasmataceae which includes these symbionts and others associated with five marine invertebrate phyla. Its exceptionally broad host range suggests that the diversity of this enigmatic family remains largely undiscovered. Oceanoplasmataceae genomes are the most highly reduced among mollicutes, providing new insight into their reductive evolution and the roles of coral symbionts.