Aryl hydrocarbon receptor (AHR) plays critical roles in various autoimmune diseases such as multiple sclerosis by controlling interleukin-17 (IL-17)–producing T-helper (T_H17) and regulatory T cells. Although various transcription factors and cytokines have been identified as key participants in T_H17 generation, the role of microRNAs in this process is poorly understood. In this study, we found that expression of the microRNA (miR)-132/212 cluster is up-regulated by AHR activation under T_H17-inducing, but not regulatory T-inducing conditions. Deficiency of the miR-132/212 cluster prevented the enhancement of T_H17 differentiation by AHR activation. We also identified B-cell lymphoma 6, a negative regulator of T_H17 differentiation, as a potential target of the miR-212. Finally, we investigated the roles of the miR-132/212 cluster in experimental autoimmune encephalomyelitis, a murine model of multiple sclerosis. Mice deficient in the miR-132/212 cluster exhibited significantly higher resistance to the development of experimental autoimmune encephalomyelitis and lower frequencies of both T_H1 and T_H17 cells in draining lymph nodes. Our findings reveal a unique mechanism of AHR-dependent T_H17 differentiation that depends on the miR-132/212 cluster.