Gut microbes are important for maintaining the intestinal barrier, and they play a role in regulating its repair. It is critical to understand the role of distinct bacteria in barrier restoration since shifts in both intestinal epithelial barrier function and microbiota composition are observed in patients with inflammatory bowel disease. GDAR2-2, a mouse commensal E. coli strain protects mice from dextran sulfate sodium-induced colitis as well as Citrobacter rodentium infection. GDAR2-2 colonization resulted in the growth of CX3CR1+ mononuclear phagocytes, along with CX3CR1+ macrophages/dendritic cells and monocytes, as well as IL-22-secreting type 3 innate lymphoid cells and betterment of epithelial barrier function. IL-1β was produced in the co-culture with macrophages. When CX3CR1+ MNPs were depleted or IL-1β and IL-22 were blocked, in vivo, protection against GDAR2-2, infection was lost. It also discovered that commensal E. coli strains that produce CX3CR1+ MNP and IL-1β in response to C. rodentium infection, suggesting they protect mice from the illness as well. The results suggest that commensal bacteria play a previously unrecognized role in promoting inflammatory IL-1β production to aid intestinal barrier repair.