Interleukin (IL)-17-producing T helper cells (T_H17) are a recently identified CD4⁺ T cell subset distinct from T helper type 1 (T_H1) and T helper type 2 (T_H2) cells. T_H17 cells can drive antigen-specific autoimmune diseases and are considered the main population of pathogenic T cells driving experimental autoimmune encephalomyelitis (EAE), the mouse model for multiple sclerosis. The factors that are needed for the generation of T_H17 cells have been well characterized^,,,. However, where and how the immune system controls T_H17 cells in vivo remains unclear. Here, by using a model of tolerance induced by CD3-specific antibody, a model of sepsis and influenza A viral infection (H1N1), we show that pro-inflammatory T_H17 cells can be redirected to and controlled in the small intestine. T_H17-specific IL-17A secretion induced expression of the chemokine CCL20 in the small intestine, facilitating the migration of these cells specifically to the small intestine via the CCR6/CCL20 axis. Moreover, we found that T_H17 cells are controlled by two different mechanisms in the small intestine: first, they are eliminated via the intestinal lumen; second, pro-inflammatory T_H17 cells simultaneously acquire a regulatory phenotype with in vitro and in vivo immune-suppressive properties (rT_H17). These results identify mechanisms limiting T_H17 cell pathogenicity and implicate the gastrointestinal tract as a site for control of T_H17 cells.