<p>All plants and animals are host to a community of microorganisms, their microbiotas, which have crucial influences on the life history and performance of their hosts. Despite the importance of such host–microbiota relationships, relatively little is known about the role microbiotas have in mediating evolution of the host and entire host–microbe assemblages. This knowledge gap is partly due to the lack of theoretical frameworks that generate testable predictions on the evolutionary dynamics of host–microbiota systems. In this Perspective, we argue that the foundation for such frameworks exists in evolutionary theory. We highlight four examples of theoretical models—niche construction, indirect genetic effects, maternal effects and multilevel selection—that capture important aspects of host–microbiome evolution. We outline how each of these frameworks can provide key insights into the evolution of host–microbiota systems while also suggesting expansions of current theory to incorporate processes unique to host–microbe assemblages; for instance, focusing on nuances in microbiota transmission and ecological microbial community dynamics. Expanding evolutionary theory to accommodate host–microbiota associations is key for a more integrative understanding of evolution, and the approach outlined here can guide future empirical research on the function and evolution of these ubiquitous interactions.</p>