Conventional dendritic cells (cDC) are key sentinels at epithelial barriers, regulating immunity to microbial pathogens and commensals while preserving tissue integrity. NOTCH2 deficiency in CD11c-expressing cells (Notch2cKO) was shown to disrupt the development of type 2a DC (cDC2a), resulting in defective intestinal TH17 response and increased susceptibility to enteropathogenic bacteria. This susceptibility contributed to the development of a persistent dysbiosis within our Notch2cKO colony, that was characterized by low-grade inflammation and systemic autoimmune features, including elevated autoantibody titers and immune-complex depositions in the kidney. Intestinal dysbiosis preceded local and systemic expansion of highly inflammatory AXL-expressing type 3 DC (AXL+inf-DC3) that formed tertiary immune structures, shifting the balance towards a chronic proinflammatory state. Notably, dysbiosis in Notch2cKO mice was defined by three dominant pathobionts and was highly transferable to WT mice. Colonization with these bacteria was sufficient to induce rapid expansion of AXL+inf-DC3 and the development of similar autoimmune features. Collectively, these findings identify a microbiota–DC axis linking epithelial barrier dysfunction to systemic autoimmunity and reveal inflammatory DC3 as a cellular bridge between dysbiosis and autoimmune pathogenesis.