Most of the immunoglobulin A (IgA) in the gut is generated by B cells in the germinal centers of Peyer's patches through a process that requires the presence of CD4⁺ follicular B helper T(T_FH) cells. The nature of these T_FH cells in Peyer's patches has been elusive. Here, we demonstrate that suppressive Foxp3⁺CD4⁺ T cells can differentiate into T_FH cells in mouse Peyer's patches. The conversion of Foxp3⁺ T cells into T_FH cells requires the loss of Foxp3 expression and subsequent interaction with B cells. Thus, environmental cues present in gut Peyer's patches promote the selective differentiation of distinct helper T cell subsets, such as T_FH cells.