Significance Microbes have a strong impact on the biology of their host, with those living in the gut being essential to immunity, development, and metabolism. A functional gut, however, has been lost several times during animal evolution. Here, using sister sea urchin species, we report that the loss of a functional gut corresponds with a reduced microbial diversity and abundance. Gut loss also coincides with associating with an endosymbiont that complements host nutrition and potentially impacts host reproduction. Therefore, transitions in developmental life histories in animals can accompany shifts in the microbial community.