Interleukin 17 (IL-17) is a central cytokine implicated in inflammation and antimicrobial defense. After infection, both innate and adaptive IL-17 responses have been reported, but the type of cells involved in innate IL-17 induction, as well as their contribution to in vivo responses, are poorly understood. Here we found that Citrobacter and Salmonella infection triggered early IL-17 production, which was crucial for host defense and was mediated by CD4⁺ T helper cells. Enteric innate T helper type 17 (iT_H17) responses occurred principally in the cecum, were dependent on the Nod-like receptors Nod1 and Nod2, required IL-6 induction and were associated with a decrease in mucosal CD103⁺ dendritic cells. Moreover, imprinting by the intestinal microbiota was fully required for the generation of iT_H17 responses. Together, these results identify the Nod-iT_H17 axis as a central element in controlling enteric pathogens, which may implicate Nod-driven iT_H17 responses in the development of inflammatory bowel diseases.