Abstract Epidemiological evidence suggests developmental exposures to certain pollutants correlate with lower antibody responses to childhood immunizations, but the mechanism by which this occurs is unknown. The transcription factor aryl hydrocarbon receptor (AhR) is activated by a variety of chemicals, expressed by immune cells, and has been shown to influence immune function, such as CD4+ T cell subset specification and function. The effect of maternal exposure to AhR ligands on the function of CD4+ T cells has never been directly examined. We report here the consequences of developmental triggering of the AhR on the CD4+ T cell response to influenza virus infection. Mice developmentally exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), the prototypical AhR ligand, have fewer activated, virus-specific CD4+ T cells, Th1, and T follicular helper cells, yet an increase in regulatory T cells in their lung draining lymph nodes. Consistent with this, developmentally exposed mice have a reduction in their class-switched, virus-specific antibody response. By using reciprocal adoptive transfers, we demonstrate that the effects of developmental activation of the AhR on CD4+ T cells occur through both direct and indirect pathways. These findings suggest changes in the functional capacity of CD4+ T cells may be a key contributor to the decreased antibody response to immunizations observed in children of mothers exposed to AhR-binding chemicals.