Cryptosporidium can cause severe diarrhea and morbidity, but many infections are asymptomatic. Here, we studied the immune response to a commensal strain of Cryptosporidium tyzzeri (Ct -STL) serendipitously discovered when conventional type 1 dendritic cell (cDC1)-deficient mice developed cryptosporidiosis. Ct -STL was vertically transmitted without negative health effects in wild-type mice. Yet, Ct -STL provoked profound changes in the intestinal immune system, including induction of an IFN-γ-producing Th1 response. TCR sequencing coupled with in vitro and in vivo analysis of common Th1 TCRs revealed that Ct -STL elicited a dominant antigen-specific Th1 response. In contrast, deficiency in cDC1s skewed the Ct -STL CD4 T cell response toward Th17 and regulatory T cells. Although Ct -STL predominantly colonized the small intestine, colon Th1 responses were enhanced and associated with protection against Citrobacter rodentium infection and exacerbation of dextran sodium sulfate and anti-IL10R-triggered colitis. Thus, Ct -STL represents a commensal pathobiont that elicits Th1-mediated intestinal homeostasis that may reflect asymptomatic human Cryptosporidium infection. [Display omitted] • Cryptosporidium tyzzeri in our colony (Ct -STL) is a commensal pathobiont • Ct -STL elicits a dominant antigen-specific Th1 response • cDC1s are required for efficient Th1 induction and blockade of Th17/Treg generation • Ct -STL markedly affects the immune system of both the small and large intestine Cryptosporidium are protozoan parasites that cause gastrointestinal illness in humans and animals worldwide. We identified a commensal strain of Cryptosporidium tyzzeri endemic in our mouse colony. This strain of Cryptosporidium does not cause disease in wild-type mice but changes the composition and function of the intestinal immune system. [ABSTRACT FROM AUTHOR]