Mucosal-Associated Invariant T (MAIT) cells are prominently localized in gastro-intestinal mucosal tissues and recognize MR1-presented microbial vitamin metabolites that are produced by both intestinal commensals and pathogens. However, very little is known about the role and function of MAIT cells during intestinal infection, which is in large part due to the low numbers of MAIT cells in commonly used laboratory mouse strains. Here, we used several mouse strains, including novel traceable MAIT T cell receptor (TCR) retrogenic (Rg) mice, iVa19 TCR transgenic mice, and wild-type mice, together with antigen-loaded MR1 tetramers to investigate the function of MAIT cells during Citrobacter rodentium infection. At steady state, intestinal MAIT cells displayed a CD44^highCD62L^neg activated/memory phenotype and expressed PLZF and T-bet. However, two populations remained distinct based on the expression of RORgt. Following in vitro C. rodentium infection, MAIT cells secreted large amounts of IFN-g, TNF-a, IL-17A and IL-22. Secretion of IFN-g and IL-17A required both activating cytokines and TCR stimulation mediated by C. rodentium antigen-loaded MR1 molecules. In contrast, efficient IL-22 release required secretion of IL-1b and IL-23 by infected antigen presenting cells and occurred in the absence of concomitant TCR ligation. In vivo, C. rodentium infection led to the rapid activation of MAIT cells and their accumulation in the colon. Importantly, early during C. rodentium infection, mice with a high frequency of MAIT cells showed significantly reduced bacterial burden. Furthermore, MAIT cell activation enhanced expression of antimicrobial peptides by intestinal epithelial cells, a key function of the intestinal barrier contributing to protective immunity. Taken together, our data suggest that MAIT cell effector functions are differentially regulated by TCR- and cytokine-mediated signals, and reveal an important contribution of MAIT cells in the early immune response to bacterial infection of the intestinal tract.