Gastro-intestinal helminth infections trigger the release of interleukin-33 (IL-33), which induces type 2 helper T-cells (Th2 cells) at the site of infection to produce IL-13, thereby contributing to host resistance in a T cell receptor (TCR)-independent manner. Here we show that as a prerequisite for IL-33 induced IL-13 secretion, Th2 cells required the expression of the Epidermal Growth Factor Receptor (EGFR) and of its ligand, Amphiregulin, for the formation of a signaling complex between T1/ST2 (the IL-33R) and EGFR. This shared signaling complex allowed IL-33 to induce the EGFR-mediated activation of the MAP-kinase signaling pathway and consequently the expression of IL-13. Lack of EGFR expression on T cells abrogated IL-13 expression in infected tissues and impaired host resistance. EGFR expression on Th2 cells was TCR-signaling dependent, and therefore our data reveal a mechanism by which antigen-presentation controls the innate effector function of Th2 cells at the site of inflammation.