Interleukin 1β (IL-1β) is critical for the in vivo survival, expansion and effector function of IL-17–producing helper T (T_H17) cells during autoimmune responses, including experimental autoimmune encephalomyelitis (EAE). However, the spatiotemporal role and cellular source of IL-1β during EAE pathogenesis are poorly defined. In the present study, we uncovered a T cell–intrinsic inflammasome that drives IL-1β production during T_H17-mediated EAE pathogenesis. Activation of T cell antigen receptors induced expression of pro-IL-1β, whereas ATP stimulation triggered T cell production of IL-1β via ASC-NLRP3–dependent caspase-8 activation. IL-1R was detected on T_H17 cells but not on type 1 helper T (T_H1) cells, and ATP-treated T_H17 cells showed enhanced survival compared with ATP-treated T_H1 cells, suggesting autocrine action of T_H17-derived IL-1β. Together these data reveal a critical role for IL-1β produced by a T_H17 cell–intrinsic ASC–NLRP3–caspase-8 inflammasome during inflammation of the central nervous system.