Fungal disease is a common cause of death worldwide (surpassing even tuberculosis), yet there are currently no anti-fungal vaccines available for humans. Effective adaptive immunity to fungi is dependent on CD4⁺ helper T cells, specifically the T_H1 and T_H17 subsets. Prior studies have shown that activation of iNKT cells via administration of glycolipids such as a-GalCer markedly enhances adaptive immune responses to protein antigens, and that this pathway promotes T_H1 responses by stimulating DC secretion of IL-12p70. We show here that exposing freshly isolated human monocytes (not pulsed with stimulatory glycolipids) to human iNKT cells results in the secretion of large quantities of IL-6 and IL-1β, cytokines known to be critical for the induction of human T_H17 cells. iNKT cells also drive the differentiation of monocyte-derived DCs that preferentially secrete these T_H17-polarizing cytokines after exposure to TLR4 or Dectin-1 ligands. Presentation of protein antigens from C. albicans or A. fumigatus by such DCs results in activation of autologous T cells to produce IL-17A. These results suggest that interaction between iNKT cells and monocytes presenting self antigens can drive a T_H17 pathway. Thus, vaccination strategies that engage iNKT cells along with the delivery of specific fungal antigens to monocytic cells may be instrumental for tailoring effective T cell responses to confer protective anti-fungal immunity.