Microbes have a critical role in the development and health of some marine invertebrate species. However, it is unclear how host-associated microbial communities are affected by climate change across host generations. Here, we use a four-year multigenerational experiment to explore microbe-host interactions under IPCC-forecast climate scenarios in the reef urchin Echinometra sp. A. Adult urchins (F0) were exposed for 18 months to increased temperature and pCO2 levels predicted for years 2050 and 2100 under RCP 8.5, and their offspring (F1, F2) were raised under parental climate treatments. Furthermore, cross-generational climate effects were explored in the F1 offspring microbiome through a reciprocal transplant experiment. Amplicon 16S rRNA gene sequence analysis was used to characterise the bacterial community across major life stages, generations and climate treatments. Each life stage and generation were associated with a distinct microbiome, with higher microbial diversity observed in juveniles compared to larval stages. Under climate treatments, we observed a variation in the urchin microbial community structure, as well as climate-mediated parental effects on the offspring microbiome. These results suggest that although the urchin microbiome varies under projected temperature and pCO2 conditions predicted for 2050 and 2100, life stage microbial specificity is maintained in this reef species.