Abstract CD4 T cell responses against Influenza A Virus (IAV) are predominantly classified as TH1, characterized by strong IFN-γ production. However, the protective role of IFN-γ is unclear, suggesting that full TH1 polarization may be dispensable for effective CD4 immunity. We test this hypothesis by analyzing transgenic CD4 T cells recognizing IAV that are deficient in the transcription factor T-bet (Tbx21−/−), the ‘master regulator’ of TH1 differentiation. 3×106 Wild-type (WT) or Tbx21−/− effector cells, primed under TH1 conditions, were transferred to naïve congenic WT mice then infected with lethal IAV. Tbx21−/− effectors protected mice, promoting similar reductions in viral titer and weight loss recovery as WT cells. However, T-bet deficiency impacted production of several cytokines by the effectors resulting in less IFN-γ and GM-CSF but more IL-2, IL-4 and IL-17. Although the peak magnitude of WT and Tbx21−/− effector responses were similar in secondary lymphoid organs, significantly fewer Tbx21−/− cells were observed in the lungs. We thus titrated effectors to 1×106 cells, to expose any potential differences in protection arising from differential lung homing. Lower effector transfer resulted in higher viral titer and delayed weight loss recovery in mice given Tbx21−/− versus WT cells. Mechanistically, Tbx21−/− cells expressed lower levels of the chemokine receptor CXCR3. CXCR3 blockade in mice given WT effectors reduced their numbers in the lungs and delayed weight loss recovery matching patterns seen in mice given Tbx21−/− effectors. Thus, while prototypical TH1 functions are dispensable for protection against IAV, T-bet-dependent chemokine responses are required to maximize anti-viral CD4 responses at the site of infection.