Dendritic cells (DCs) in peripheral organs are key players in orchestrating complex immune responses, traditionally recognized for their role in detecting and presenting antigens to T cells. Recent studies have also highlighted their pivotal role in the central nervous system (CNS), although their specific contribution to CNS-specific immune regulation remains under debate. In this study, we employ high-dimensional single-cell immune profiling and novel fate- mapping models to investigate the role of a subset of DCs, the migratory DCs (migDCs), in CNS immunity. Our findings reveal that migDCs function as essential connectors between the CNS and the peripheral immune system. Under both steady-state and CNS-damage, migDCs actively phagocytose CNS-derived antigens and subsequently migrate from the CNS to the peripheral draining lymph nodes (LNs), where they present these antigens to naïve T cells. When we interfered with their migratory and/or immunregulatory capacity, we observed an accumulation of activated CD8 T cells in the CNS. In the experimental autoimmune encephalomyelitis (EAE) mouse model, this also resulted in a marked delay in the onset of clinical symptoms, highlighting their critical role in priming and recruiting pathogenic T cells to the CNS. Collectively, these data highlight a previously unexplored role for migDCs in the CNS and provide further insight into the mechanisms underlying immune regulation in the CNS, particularly during autoimmune conditions.