Abstract Toxoplasma gondii is an intracellular protozoan parasite that causes chronic brain infection in a wide range of mammalian hosts. Animal studies have demonstrated that continuous T cell recruitment to the brain is necessary for parasite control. However, it has remained unclear how T cells outside the central nervous system sense and respond to brain-derived microbial antigen. Here, we test the hypothesis that the newly described meningeal lymphatic system promotes T cell immunity during T. gondii brain infection. We find that chronic brain infection is associated with significant expansion of parasite-specific T cells in the cerebrospinal fluid (CSF)-draining deep cervical lymph nodes. T cell activation at this site is correlated with parasite burden in the brain and peaks during the late stages of chronic infection. Flow cytometric analysis of CSF reveals a population of activated dendritic cells that is not present in the CSF of naĂŻve mice. Mature dendritic cells are also mobilized in the meninges, specifically in areas where CSF protein can be sampled. Disrupting meningeal lymphatic drainage by ligating the collecting vessels leads to impaired T cell responses in the deep cervical lymph nodes. Surprisingly, in spite of reduced T cell activation and IFN-Îł production at this site, T cell responses in the brain remain intact, likely due to ongoing antigenic stimulation in lymph nodes that drain non-central nervous system tissue. Overall, we provide evidence that meningeal lymphatic drainage supports robust parasite-specific T cell responses in the deep cervical lymph nodes. Nonetheless, we find that drainage of central nervous system material to this site is dispensable for host-protective T cell responses in the brain. Supported by grants from NIH (5T32AI007496, 5T32GM007267, R01NS091067, R01NS112516, R56NS106028, F30AI154740)