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Dendritic cells (DCs) are central regulators of the delicate balance between protective immune responses to pathogens and cancer, and immunopathology. This review explores the phenotypic and functional heterogeneity of DCs and their specialized roles in regulating the immune response, with a focus on pathways that confer tolerogenic properties to DCs. Furthermore, we discuss emerging strategies for the therapeutic induction of a tolerogenic phenotype in DCs in the setting of autoimmune diseases. A better understanding of the molecular mechanisms that control the tolerogenic phenotype of DCs may open new avenues for the development of efficacious and safe immunotherapies for autoimmune, allergic, and chronic inflammatory diseases.