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Effective coral restoration must include comprehensive investigations of the targeted coral community that consider all aspects of the coral holobiont—the coral host, symbiotic algae, and microbiome. For example, the richness and composition of microorganisms associated with corals may be indicative of the corals’ health status and thus help guide restoration activities. Potential differences in microbiomes of restoration corals due to differences in host genetics, environmental condition, or geographic location, may then influence outplant success. The objective of the present study was to characterize and compare the microbiomes of apparently healthy Acropora cervicornis genotypes that were originally collected from environmentally distinct regions of Florida’s Coral Reef and sampled after residing within Mote Marine Laboratory’s in situ nursery near Looe Key, FL (USA) for multiple years. By using 16S rRNA high-throughput sequencing, we described the microbial communities of 74 A. cervicornis genotypes originating from the Lower Florida Keys ( n  = 40 genotypes), the Middle Florida Keys ( n  = 15 genotypes), and the Upper Florida Keys ( n  = 19 genotypes). Our findings demonstrated that the bacterial communities of A. cervicornis originating from the Lower Keys were significantly different from the bacterial communities of those originating from the Upper and Middle Keys even after these corals were held within the same common garden nursery for an average of 3.4 years. However, the bacterial communities of corals originating in the Upper Keys were not significantly different from those in the Middle Keys. The majority of the genotypes, regardless of collection region, were dominated by Alphaproteobacteria, namely an obligate intracellular parasite of the genus Ca. Aquarickettsia . Genotypes from the Upper and Middle Keys also had high relative abundances of Spirochaeta bacteria. Several genotypes originating from both the Lower and Upper Keys had lower abundances of Aquarickettsia , resulting in significantly higher species richness and diversity. Low abundance of Aquarickettsia has been previously identified as a signature of disease resistance. While the low- Aquarickettsia corals from both the Upper and Lower Keys had high abundances of an unclassified Proteobacteria, the genotypes in the Upper Keys were also dominated by Spirochaeta . The results of this study suggest that the abundance of Aquarickettsia and Spirochaeta may play an important role in distinguishing bacterial communities among A. cervicornis populations and compositional differences of these bacterial communities may be driven by regional processes that are influenced by both the environmental history and genetic relatedness of the host. Additionally, the high microbial diversity of low- Aquarickettsia genotypes may provide resilience to their hosts, and these genotypes may be a potential resource for restoration practices and management.