Cryptosporidium species can cause sporadic waterborne diarrhea outbreaks but infections can be a significant cause of morbidity and mortality in malnourished children and individuals with primary or acquired defects in T cell function. There is no vaccine for Cryptosporidium and the only FDA-approved therapy is ineffective in individuals most at risk of severe disease. Cryptosporidium infects epithelial cells of the small intestine, where it completes its entire lifecycle. Resistance requires the cytokine interferon-gamma (IFN-γ) and CD4+ T cells, and a prominent CD4+ T cell-dependent but IFN-γ-independent mechanism of control exists that has been a challenge to uncover. To understand the regulation of CD4+ T cell responses against Cryptosporidium, we engineered transgenic parasites to express MHCII-restricted model antigens, allowing the tracking of antigen-specific responses against a parasite-derived peptide. Using this strain coupled with tetramers and TCR transgenic mice revealed that CD4+ T cells produce protective IFN-γ locally within the gut to restrict the parasite. Type 1 conventional dendritic cells (cDC1s) were a major source of IL-12p40 during infection, and were required for CD4+ T cell gut-homing and chemokine receptor expression. However, IL-12 was not required for gut-homing but instead promoted expression of Ifng by Cryptosporidium-specific CD4+ T cells within the gut. Depletion of CD4+ lymphocytes or IL-12/23p40 in Ifng-/- mice impaired chronic control of infection, suggesting that IFN-γ-independent control of Cryptosporidium infection is dependent on both of these components of the immune system. Both CD4+ lymphocytes and IL-12/23p40 were required for induction of the cytokine IL-22, which was up-regulated during infection in type 3 innate lymphoid cells ILC3s. IL-22 protected mice from Cryptosporidium infection independent of IFN-γ and promoted the expression of STAT3- but not STAT1-target genes in epithelial cells. Protection by IL-22 was additionally independent of STAT1, revealing an IL-22-STAT3 arm of control against Cryptosporidium infection that is dependent on CD4+ lymphocytes and is independent of IFN-γ. Our studies provide a new characterization of how protective CD4+ T cells are generated against Cryptosporidium and suggest that promoting IL-22 production by ILC3s is a protective function of these critical cells.