Basophils are a rare population of granulocytes that have long been associated with IgE-mediated and Th2-associated allergic diseases. However, the role of basophils in Th17 and/or Th1 diseases has not been reported. In the present study, we report that basophils can be detected in the mucosa of Th17-associated lung and inflammatory bowel disease and accumulate in inflamed colons containing large quantities of IL-33. We also demonstrate that circulating basophils increased memory Th17 responses. Accordingly, IL-3– or IL-33–activated basophils amplified IL-17 release in effector memory T cells (T_EM), central memory T cells (T_CM), and CCR6⁺ CD4 T cells. More specifically, basophils promoted the emergence of IL-17⁺IFN-γ⁻ and IL-17⁺IFN-γ⁺, but not IL-17⁻IFN-γ⁺ CD4 T cells in T_EM and T_CM. Mechanistic analysis revealed that the enhancing effect of IL-17 production by basophils in T_EM involved the ERK1/2 signaling pathway, occurred in a contact-independent manner, and was partially mediated by histamine via H₂ and H₄ histamine receptors. The results of the present study reveal a previously unknown function for basophils in augmenting Th17 and Th17/Th1 cytokine expression in memory CD4 T cells. Because basophils accumulated in inflamed inflammatory bowel disease tissues, we propose that these cells are key players in chronic inflammatory disorders beyond Th2.