The coral reef crisis has influenced research for over two decades, during which time the capacity of corals to withstand and respond to environmental stress has been documented from the cellular to ecosystem level. Over the past decade, research is increasingly working towards uncovering the extent of coral–bacterial interactions, finding that diverse and stable microbial interactions can be indicative of the health of the coral host. However, we have yet to determine at which level of organismal organisation these interactions occur, in particular those with the coral’s photosynthetic dinoflagellate symbionts. This information is critical if we are to understand the impact of stress on meta-organism functioning. Using 16S gene amplicon sequencing, we investigated the bacterial microbiome of endosymbiotic Symbiodiniaceae from thermally stressed Acropora aspera, under 3 ecologically relevant temperature trajectories (defined as protective, repetitive and single) that are expected under a changing climate. We show that endosymbiotic Symbiodiniaceae host a distinct and diverse bacterial assemblage when compared with the A. aspera host. Alphaproteobacteria (mainly Rhodobacteraceae and Bradyrhizobiaceae), from the Rhizobiales order dominated the Symbiodiniaceae microbiome, while Gammaproteobacteria (mainly Endozoicomonadaceae) dominated the coral microbiome. The Symbiodiniaceae core microbiome also reflected the distinct microbiomes of the two partners, specifically, Rhizobiales were not present in the A. aspera core, while Endozoicomonadaceae were not present in the Symbiodiniaceae core. We show the Symbiodiniaceae-associated microbiome was highly responsive to increases in temperature, and the microbial consortium was significantly altered in the Symbiodiniaceae retained in the host exposed to different temperature. Most notably, Myxococcolaes were up to 25-fold higher relative abundance in dinoflagellate partner microbiomes under the single temperature trajectory, compared with the repetitive and control treatments. The distinct composition of bacteria associated with Symbiodiniaceae suggests a previously unrecognised, yet important functional role of these associations to overall coral health, which is increasingly important as reefs decline worldwide. Our study provides the first characterisation of Symbiodiniaceae-associated microbes from a coral host under a range of temperature trajectories occurring on the Great Barrier Reef.