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Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease‐resistant and ‐susceptibleAcropora cervicorniscoral genotypes (hereafter referred to simply as ‘genotypes’) before and after high temperature‐mediated bleaching. We found that the intracellular bacterial parasite ‘Ca.Aquarickettsia rohweri’ was strikingly abundant in disease‐susceptible genotypes. Disease‐resistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of ‘Ca.Aquarickettsia’.Bleaching caused a dramatic reduction of ‘Ca.Aquarickettsia’ within disease‐susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that ‘Ca.Aquarickettsia’ species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host‐symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress.