Intestinal Peyer's patches are essential lymphoid organs for the generation of T cell–dependent immunoglobulin A (IgA) for gut homeostasis. Through the use of interleukin 17 (IL-17) fate-reporter mice, we found here that endogenous cells of the T_H17 subset of helper T cells in lymphoid organs of naive mice 'preferentially' homed to the intestines and were maintained independently of IL-23. In Peyer's patches, such T_H17 cells acquired a follicular helper T cell (T_FH cell) phenotype and induced the development of IgA-producing germinal center B cells. Mice deficient in T_H17 cells failed to generate antigen-specific IgA responses, which provides evidence that T_H17 cells are the crucial subset required for the production of high-affinity T cell–dependent IgA.