Mechanisms by which DCs initiate Th2 responses and the role for DCs throughout allergic memory responses are not completely understood. We previously demonstrated that expression of the transcription factor IRF4 in mature DCs is needed for type 2 lung inflammation in response to house dust mite extract (HDM) in mice. We hypothesized that IRF4 regulates specific functions in mature DCs that are required for Th2 induction and lung resident memory T cell (TRM) responses. Here, we demonstrate that mice having IRF4-deficient DCs display impaired recruitment of activated effector T cells to the lung soon after sensitization. While IRF4-deficient DCs exhibit minimal defects in the lungs, we find that their migration to the draining lymph nodes is limited. Moreover, DC-intrinsic defects in Th2 priming exist. IRF4-deficient DCs express less of the Th2-associated costimulatory molecule OX40L and less of the Th2-promoting cytokines IL-33 and IL-10. The instillation of IL-33 and IL-10 into the lungs during sensitization restores T cell production of some Th2 cytokines but does not entirely restore inflammation, suggesting other effector molecules downstream of IRF4 play an important role in initiating the Th2 response. Further, we demonstrate that mice lacking IRF4-expressing DCs during sensitization display impaired memory responses to HDM, but T cells educated by IRF4-competent DCs mediate potent memory responses independently of IRF4-expressing DCs. Together, these findings suggest that IRF4 controls a program in mature DCs that governs Th2 priming during sensitization and Th2 effector responses during challenge, but that mitigated TRM-dependent responses stem from defects in earlier education.