Soluble oat fibers, including β-glucan, have been shown to alter the gut microbiome composition and ameliorate DSS-induced colitis; however, the beneficial effect of soluble oat fiber on colonic inflammation is not yet fully understood. In this study, we demonstrated that soluble oat fibers ameliorate T cell-dependent colitis through the induction of peripherally induced regulatory T cells (pTregs). Soluble oat fibers elevated colonic butyrate production dose-dependently, which coincided with the overrepresentation of Faecalibaculum rodentium (an analog of butyrate-producing Holdemanella biformis) in the gut microbiome. Soluble oat fibers promoted the growth of F. rodentium and H. biformis even in vitro, and increased the concentration of butyrate in the culture supernatant. These results indicate that soluble oat fibers are an energy source for butyrate-producing bacteria and are a fermentation substrate. Soluble oat fibers increased the percentage of colonic pTregs and ameliorated the weight loss and inflammation in acute 2,4,6-trinitrobenzenesulfonic acid (TNBS)-induced colitis; this may in part be mediated by the increase in IL-10-producing T cells. In conclusion, our results suggest that the administration of soluble oat fibers is a promising prebiotic treatment for the prevention of colitis mediated via altered gut microbiota composition and elevated butyrate production.