ABSTRACT Insect guts house a complex community of microbes that affect host physiology, performance and behavior. Gut microbiome research has largely focused on bacteria–host symbioses and paid less attention to other taxa, such as yeasts. We found that axenic Drosophila melanogaster (reared free of microbes) develops from egg to adult more slowly (ca. 13 days) than those with a natural microbiota (ca. 11.5 days). Here, we showed that live yeasts are present and reproducing in the guts of flies and that the fast development time can be restored by inoculating larvae with a single yeast species (either Saccharomyces cerevisiae or Lachancea kluyveri). Nutritional supplements (either heat-killed yeasts, or a mix of essential vitamins and amino acids) slightly sped the development of axenic flies (to ca. 12.5 days), but not to the same extent as live yeasts. During the first two instars, this acceleration appears to result from additional macronutrient availability, but during the third instar, when most growth occurs, live yeasts increased feeding rate, implying an effect mediated by the gut–brain axis. Thus, the fly–yeast interaction extends beyond yeasts-as-food to yeasts as beneficial interactive symbionts.