T helper 17 (Th17) cells play crucial roles in protective immunity to extracellular bacterial/fungal infections, but also drive pathogenesis of numerous experimental autoimmune pathologies, including the mouse model of multiple sclerosis (MS), experimental autoimmune encephalomyelitis (EAE). Two types of Th17 cells have been reported: ‘regulatory’ Th17 cells which co-express the immunomodulatory cytokines IL-2/IL-9/IL-10; and ‘pathogenic’ Th17 cells, which require IL-23 and T-Bet for differentiation and co-express the proinflammatory cytokines GM-CSF and IFN-γ. However, evidence for the existence of these two Th17 subsets in vivo remains controversial. Th17 trafficking to the CNS during EAE is described to occur in two waves: the first wave driven by CCR6 facilitates entry into the uninflamed CNS and initiates inflammation, followed by a CCR6-independent wave driving recruitment of these cells into the inflamed CNS. Using novel KO animals, bone-marrow chimeras, antagonists and Th17 transfer systems, we identify CCR2 as the crucial chemokine receptor which facilitates the second wave of encephalitogenic Th17 cell recruitment to the CNS during EAE. The emergence of CCR2+ Th17 cells occurs late during Th17 priming with the earliest CNS-infiltrating Th17 cells bearing a CCR6+CCR2- phenotype followed by the advent of CCR6+CCR2+ and CCR6-CCR2+ Th17 cells late during disease progression. Th17 cells bearing the CCR6-CCR2+ phenotype express high levels of the transcription factor T-Bet and lower levels of RORγt, c-Maf, AHR, IRF4 and IRF8; are the only Th17 cells to express GM-CSF and IFN-γ and their differentiation was dependent on IL-23, IL-1, TNF-α and IFN-γ. Thus, ‘pathogenic’ Th17 cells bear a CCR6-CCR2+ phenotype in vivo and are recruited to the inflamed CNS via CCR2.