The intestinal immune system maintains tolerance to harmless food proteins and gut microbiota through peripherally derived RORgammat(+) Tregs (pTregs), which prevent food intolerance and inflammatory bowel disease. Recent studies suggested that RORgammat(+) antigen-presenting cells (APCs), which encompass rare dendritic cell (DC) subsets and type 3 innate lymphoid cells (ILC3s), are key to pTreg induction. Here, we developed a mouse with reduced RORgammat(+) APCs by deleting a specific cis-regulatory element of Rorc encoding RORgammat. Single-cell RNA sequencing and flow cytometry analyses confirmed the depletion of a RORgammat(+) DC subset and ILC3s. These mice showed a secondary reduction in pTregs, impaired tolerance to oral antigens, and an increase in T helper (Th)2 cells. Conversely, ILC3-deficient mice showed no pTregs or Th2 cell abnormalities. Lineage tracing revealed that RORgammat(+) DCs share a lymphoid origin with ILC3s, consistent with their similar phenotypic traits. These findings highlight the role of lymphoid RORgammat(+) DCs in maintaining intestinal immune balance and preventing conditions like food allergies.