The microbiota has been recognized as a critical contributor to various diseases(1), with multiple reports of changes in the composition of the gut microbiome in contexts such as inflammatory bowel disease(2,3) and neurodegenerative diseases(4). These microbial shifts can exert systemic effects by altering the release of specific metabolites into the bloodstream(5,6), and the gastrointestinal microbiota has also been reported to exhibit immunomodulatory activity through the activation of innate and adaptive immunity(7,8). However, it remains unclear how the microbiota contributes to inflammation in the central nervous system (CNS), where these microorganisms are typically absent. Here we report that T cells that recognize gut-colonizing segmented filamentous bacteria can induce inflammation in the mouse intestine and CNS in the absence of functional regulatory T cells. Gut commensal-specific CD4 T cells (T(comm) cells) that are dysregulated in the inflamed gut can become licensed to infiltrate into the CNS regardless of their antigen specificity and have the potential to be re-stimulated by host protein-derived antigens in the CNS via molecular mimicry, whereupon they produce high levels of GM-CSF, IFNgamma and IL-17A, triggering neurological damage. These infiltrated T(comm) cells initiate CNS inflammation by activating microglia through their IL-23R-dependent encephalitogenic programme and their IL-23R-independent GM-CSF production. Together, our findings reveal potential mechanisms whereby perturbation of T(comm) cells can contribute to extraintestinal inflammation.