The intestinal immune system facilitates nutrient absorption in the presence of diverse commensal microbiota while establishing a protective barrier to prevent infection. Prototypically studied microbes induce specific immune programs and these models provide insight into how the immune system is regulated in this unique environment. Tritrichomonas species are protozoan symbionts that are common in many mouse facilities. These protozoa typically induce a type-2 immune program in the small intestine characterized by interleukin-25 (IL-25) signaling and secretory cell hyperplasia that is primarily mediated through the action of GATA3+ innate lymphocytes (ILC2s). However, unlike immunity to helminths, for which the type 2 immune program is evolved, this immune response is self-limiting; a state of tolerance is developed whereby the protozoa continue to occupy the lumen without continued immune activation or adaptive memory formation. We previously identified small intestinal barrier dysfunction correlated with increased IL-25 signaling in mice deficient for the DNA methylcytosine dioxygenase TET2. In these mice, Tritrichomonas colonization induces a population of long-lived adaptive CD4 T lymphocytes expressing GATA3 (Th2 cells) that chronically propagate this IL-25 circuit. Naïve lymphocytes typically require paracrine interleukin-4 (IL-4) from various innate populations for efficient Th2 differentiation in helminth infections. Tet2-deficient naïve cells are able to make increased autocrine IL-4, which results in Th2 polarization even in the absence of helminth induced innate activation. In a model of peanut allergy, loss of TET2 predisposed mice to anaphylaxis. Collectively, our findings formally demonstrate that a cell-intrinsic checkpoint can prevent exacerbated immune responses at homeostasis in the microbe- and stimulus-rich intestinal environment.