Intestinal Peyer’s patches are essential lymphoid organs for the generation of T cell-dependent immunoglobulin (Ig) A production for gut homeostasis. Using IL-17 fate reporter mice we show here that endogenous T H17 cells in lymphoid organs of naïve mice home preferentially to the intestine and are maintained independently of IL-23. In Peyer’s patches such T H17 cells acquire a T follicular helper (T FH) phenotype and induce the development of IgA-producing germinal center B cells. Mice deficient in T H17 cells fail to generate antigen specific IgA responses, providing evidence that T H17 cells are the crucial subset required for high affinity T cell-dependent IgA production.