As the most diverse vertebrate group and a major component of a growing global aquaculture industry, teleosts continue to attract significant scientific attention. The growth in global aquaculture, driven by declines in wild stocks, has provided additional empirical demand, and thus opportunities, to explore teleost diversity. Among key developments is the recent growth in microbiome exploration, facilitated by advances in high-throughput sequencing technologies. Here, we consider studies on teleost gut microbiomes in the context of sustainable aquaculture, which we have discussed in four themes: diet, immunity, artificial selection and closed-loop systems. We demonstrate the influence aquaculture has had on gut microbiome research, while also providing a road map for the main deterministic forces that influence the gut microbiome, with topical applications to aquaculture. Functional significance is considered within an aquaculture context with reference to impacts on nutrition and immunity. Finally, we identify key knowledge gaps, both methodological and conceptual, and propose promising applications of gut microbiome manipulation to aquaculture, and future priorities in microbiome research. These include insect-based feeds, vaccination, mechanism of pro- and prebiotics, artificial selection on the hologenome, in-water bacteriophages in recirculating aquaculture systems (RAS), physiochemical properties of water and dysbiosis as a biomarker.