Intraepithelial lymphocytes expressing the gammadelta T cell receptor (gammadelta IELs) provide immunosurveillance of the intestinal barrier but are reduced in patients with active Crohn's disease (CD). Here, we report an underappreciated role for gammadelta IELs in maintaining immunological tolerance during the onset and progression of CD-like ileitis using TNF(DeltaARE/+) mice. We found that TNF-induced down-regulation of epithelial hepatocyte nuclear factor 4-gamma/butyrophilin is followed by a loss of ileal Vgamma7 IELs and impaired barrier surveillance before the histological onset of disease. A reduction of immunoregulatory CD39(+) gammadelta IELs coincided with the influx of immature, peripheral CD39(neg) gammadelta T cells into the epithelium, leading to an expansion of induced IELs, whereas an earlier depletion of gammadelta IELs correlated with accelerated onset of ileal inflammation. Our findings identify multiple layers of gammadelta IEL dysregulation before ileitis development, indicating that the loss of steady-state immunoregulatory gammadelta IELs may contribute to the initiation of ileal CD.