Mucosal-associated invariant T-cells (MAIT cells) recognize MR1-presented riboflavin metabolites produced by commensals and intestinal microbes. Mounting evidence positions them as potent unconventional T-cell subset with numerous immune functions. Given their abundance in the gastrointestinal tract, MAIT cells are likely to play a central role in modulating intestinal immunity. However, our understanding of their role in intestinal immunity needs further exploration. Using the Citrobacter rodentium (C.r) model of intestinal infection and RNA-sequencing of MAIT cells in lamina propria (LPL) and spleen (SPL), we assessed the role of MAIT cells in different environments. In-vitro stimulation of MAIT cells with Citrobacter antigens led to rapid activation and secretion of cytokines such as IFN-g, TNF-a, IL-17A, and IL-22. Additionally, activated MAIT cells enhanced the expression of antimicrobial peptides from intestinal epithelial cells. Similarly, in vivo, activation of MAIT cells following C. rodentium infection resulted in better resolution of infection in iVa19TCR-MR1+/+ mice, and lack of MAIT cells resulted in more severe disease with higher bacterial loads in iVa19TCR- MR1-/- mice. On transcriptional profiling, we identified distinct MAIT cells in LPL and SPL at baseline and during C.r infection. Unexpectedly, the SPL MAIT cells had a more dynamic profile than the LPL during infection. The similarity in LPL MAIT cells in both conditions indicates a common gene expression profile independent of infection state. Furthermore, GSEA analysis showed significant enrichment of tissue repair functionality in LPL at baseline, suggesting a vital role for MAIT cells in intestinal homeostasis. We also identified the expression of various neurotransmitter receptors like Adora2a and P2rx7 on MAIT cells that need in-depth evaluation. Together, these findings advance our understanding of MAIT cell role in intestinal immune responses during homeostasis and disease, which may help unlock their therapeutic potential.