The question of which dendritic cells (DCs) respond to pulmonary antigens and cross-prime CD8⁺ T cells remains controversial. We show here that influenza-specific CD8⁺ T cell priming was controlled by different DCs at different times after infection. Whereas early priming was controlled by both CD103⁺CD11b^lo and CD103⁻CD11b^hi DCs, CD103⁻CD11b^hi DCs dominated antigen presentation at the peak of infection. Moreover, CD103⁻CD11b^hi DCs captured exogenous antigens in the lungs and directly cross-primed CD8⁺ T cells in the draining lymph nodes without transferring antigen to CD8α⁺ DCs. Finally, we show that CD103⁻CD11b^hi DCs were the only DCs to express CD70 after influenza infection and that CD70 expression on CD103⁻CD11b^hi DCs licensed them to expand CD8⁺ T cell populations responding to both influenza and exogenous ovalbumin.