The transcription factor T-bet has been associated with increased susceptibility to systemic and organ-specific autoimmunity, but the mechanism by which T-bet expression promotes neuroinflammation remains unknown. In this study, we demonstrate a cardinal role of T-bet-dependent NKp46⁺ innate lymphoid cells (ILCs) in the initiation of CD4⁺ T_H17-mediated neuroinflammation. Loss of T-bet specifically in NKp46⁺ ILCs profoundly impaired the ability of myelin-reactive T_H17 cells to invade central nervous system (CNS) tissue and protected the mice from autoimmunity. T-bet-dependent NKp46⁺ ILCs localized in the meninges and acted as chief coordinators of meningeal inflammation by inducing the expression of proinflammatory cytokines, chemokines and matrix metalloproteinases, which together facilitated T cell entry into CNS parenchyma. Our findings uncover a detrimental role of T-bet-dependent NKp46⁺ ILCs in the development of CNS autoimmune disease.