Interleukin (IL) 17–producing T helper (T_H17) cells have been selected through evolution for their ability to control fungal and bacterial infections. It is also firmly established that their aberrant generation and activation results in autoimmune conditions. Using a characterized potent and selective small molecule inhibitor, we show that the bromodomain and extra-terminal domain (BET) family of chromatin adaptors plays fundamental and selective roles in human and murine T_H17 differentiation from naive CD4⁺ T cells, as well as in the activation of previously differentiated T_H17 cells. We provide evidence that BET controls T_H17 differentiation in a bromodomain-dependent manner through a mechanism that includes the direct regulation of multiple effector T_H17-associated cytokines, including IL17, IL21, and GMCSF. We also demonstrate that BET family members Brd2 and Brd4 associate with the Il17 locus in T_H17 cells, and that this association requires bromodomains. We recapitulate the critical role of BET bromodomains in T_H17 differentiation in vivo and show that therapeutic dosing of the BET inhibitor is efficacious in mouse models of autoimmunity. Our results identify the BET family of proteins as a fundamental link between chromatin signaling and T_H17 biology, and support the notion of BET inhibition as a point of therapeutic intervention in autoimmune conditions.