Influenza B infection is an important source of morbidity and mortality, especially in vulnerable populations such as children. Improved vaccines and antiviral therapeutics are hindered by gaps in knowledge about influenza B viruses (IBVs). We examined the immune responses in the lung, at the kinetic interface between the innate and adaptive response with a focus on the CD4 T-cell response to infection. Using a mouse model of infection with influenza A virus (IAV) A/California/04/2009 and influenza B virus (IBV) B/Brisbane/60/2008, striking differences in early cytokines and chemokines associated with induction of Th1-biased immune responses were identified. Quantifying these mediators on a temporal basis, IBV infection leads to earlier lung expression of the cytokines IFN-γ, IP-10, and MIP1-B in the lung relative to IAV. Given the critical role for IFN-γ in antiviral responses, the use of direct ex vivo cytokine staining and multiparameter flow cytometry revealed that, at day 6 after infection, when lung lysates contained the highest levels of IFN-γ, significant differences were found in the abundance of IFN-γ–producing Ly6C+ monocytes, CD4 T cells, and CD8 T cells in the IBV–infected lung, but not the IAV-infected lung. Data from a reporter mouse model of T-cell receptor engagement, epitope-specific cytokine enzyme-linked immunospot assays, quantitative lung cytokine abundance, and earlier viral clearance suggest a distinctive mechanism of IBV and IAV responses whereby the kinetics in recruitment of epitope-specific T cells to the IBV-infected lung is driven by early innate responses and leads to more rapid viral clearance.