Summary Capsular polysaccharides (CPS) play multiple roles in protecting bacteria from host and environmental factors, and many commensal bacteria can produce multiple capsule types. To better understand the roles of different CPS in competitive intestinal colonization, we individually expressed the eight different capsules of the human gut symbiont Bacteroides thetaiotaomicron. Certain CPS were most advantageous in vivo, and increased anti-CPS IgA correlated with increased fitness of a strain expressing one particular capsule CPS5, suggesting that it promotes avoidance of adaptive immunity. A strain with the ability to switch between multiple capsules was more competitive than those expressing any single capsule except CPS5. After antibiotic perturbation, only the wild-type, capsule-switching strain remained in the gut, shifting to prominent expression of CPS5 only in mice with intact adaptive immunity. These data suggest that different capsules equip mutualistic gut bacteria with the ability to thrive in various niches, including those influenced by immune responses and antibiotic perturbations.