Whooping cough, caused by Bordetella pertussis (Bp), is a highly contagious respiratory disease. Pertussis toxin (PTX) is largely responsible for extreme leukocytosis and chronic disease. Th17 cells have been implicated in host defense and control of mucosal pathogens, including Bp. Plasmacytoid dendritic cells (pDCs) have been shown to participate in Th17 commitment through secretion of IL-6. However, stimulation of pDCs through Toll-like receptor 7 leads to the secretion of IFN-α, a cytokine documented to inhibit Th17 differentiation. pDCs are activated during lung inflammation in response to pathogens, but their role during Bp infection is understudied. Using murine infection models of Bp and BpΔPTX (Bp strain devoid of PTX), we test the hypothesis that the functions of pDCs can manipulate the rise of Th17 cells during infection. Lung Th17 cells increase significantly in Bp-infected mice only by 10 days post-infection (p.i.), while lung pDCs emerged 2-3 fold at 5 days p.i. During the late rise in Th17 cells, the frequency of pDCs secreting IFN-α drops while those secreting IL-6 increase. In addition, blocking IFN-α production in mice results in an earlier increase in Th17 cells during infection. The recruitment and cytokine secretion of lung pDCs during infection with Bp correlate with the delayed Th17 responses, suggesting a role for pDCs in Th17 differentiation that may account for a longer-lasting disease.