Corals associate with a diverse community of prokaryotic symbionts that provide nutrition, antioxidants, and other protective compounds to their host. However, the influence of microbes on coral thermotolerance remains understudied. Here, we examined the prokaryotic microbial communities associated with colonies of Acropora cf. tenuis that exhibit high or low thermotolerance upon exposure to 33°C (heated) relative to 29°C (control). Using 16S rRNA sequencing, we show that the microbial community structure of all A. cf. tenuis colonies were similar at control temperature. Thermotolerant colonies, however, had relatively greater abundance of Endozoicomonas, Arcobacter, Bifidobacterium and Lactobacillus. At elevated temperature, only thermosensitive colonies showed a distinct shift in their microbiome, with an increase in Flavobacteriales, Rhodobacteraceae, and Vibrio, accompanying a marked bleaching response. Functional prediction indicated that prokaryotic communities associated with thermotolerant corals were enriched for genes related to metabolism, while microbiomes of thermosensitive colonies were enriched for cell motility and antibiotic compound synthesis. These differences may contribute to the variable performance of thermotolerant and thermosensitive corals under thermal stress. Identification of microbial taxa correlated with thermotolerance provides insights into beneficial bacterial groups that could be used for microbiome engineering to support reef health in a changing climate.