The contribution of different DC subsets to effector and memory CD8⁺ T cell generation during infection and the mechanism by which DCs controls these fate decisions is unclear. Here we demonstrated that the CD103⁺ and CD11b^hi migratory respiratory DC (RDC) subsets after influenza virus infection activated naive virus-specific CD8⁺ T cells differentially. CD103⁺ RDCs supported the generation of CD8⁺ T effector (Teff) cells, which migrate from lymph nodes to the infected lungs. In contrast, migrant CD11b^hi RDCs activated CD8⁺ T cells characteristic of central memory CD8⁺ T (CD8⁺ Tcm) cells including retention within the draining lymph nodes. CD103⁺ RDCs expressed CD24 at an elevated level, contributing to the propensity of this DC subpopulation to support CD8⁺ Teff cell differentiation. Mechanistically, CD24 was shown to regulate CD8⁺ T cell activation through HMGB1-mediated engagement of T cell RAGE. Thus, there is distribution of labor among DC subsets in regulating CD8⁺ T cell differentiation.