The advent of highly-refined wheat products has contributed to reduced fiber consumption, which is associated with increased risk for inflammatory bowel disease (IBD). This led us to investigate whether enriching diets with wheat fiber (WF) impacts proneness to experimental colitis. Indeed, WF protected mice against dextran sodium salt (DSS)-induced acute colitis, especially relative to a low-fiber diet (LF), as demonstrated across clinical, histopathologic, morphologic, and immunologic parameters. Notably, WF-mediated protection was independent of short-chain acids (SCFA), but associated with preservation of microbiota diversity, including maintenance of Bacteroides thetaiotaomicron (B. theta), which was necessary and sufficient for WF’s protective effect. B. theta’s presence in gnotobiotic mice harboring Altered Schaedler Flora (ASF) consortium enabled WF-induced production of fecal metabolites, including plant-derived polyphenol isofraxidin, which reprogrammed macrophages towards an M2-like phenotype. Metabolic and phenotypic reprogramming of macrophages ex vivo via WF-induced metabolites, followed by their adoptive transfer into mice, recapitulated WF’s protection against colitis. Additionally, we tested the impact of WF in a chronic T-cell-transfer colitis model, where Rag1-/- mice were fed either LF or WF diets and then administered CD45Rbhi T-cells. WF conferred robust protection as assessed by an array of clinical, histopathologic, morphologic, and immune-related parameters. This protection was associated with a microbiota-dependent increase in Foxp3+ regulatory T cells (Tregs), which could be recapitulated in vitro. However, WF did not increase Tregs in mice lacking conserved non-coding sequence 1 (CNS1), which is essential for peripheral Treg (pTreg) development, nor did WF protect against T-cell-transfer colitis driven by transplant of colitogenic T-cells from CNS1-/- mice, suggesting that pTregs are required for WF-mediated protection. Together, these findings indicate that WF reduces intestinal inflammation through microbiota-dependent reprogramming of macrophages and peripheral Treg induction, thereby suggesting potential mechanisms by which WF consumption may mitigate the development of IBD.