Inhaled agents pose a challenge to immunological homeostasis in the respiratory tract, requiring constant screening for their potential risk to the host. Previous studies indicate that this requires a balanced network of dendritic cells (DC) subsets in the mucosal and parenchymal lung compartments that regulate T cell tolerance or immunity, both locally and in draining lymph nodes. Influenza A virus infection poses a serious threat of disrupting this fine balance due to damage to epithelial barriers and its potent inflammatory and cytotoxic activities. In this study, we used a BALB/c mouse, A/PR8/34 H1N1 Influenza Type A Virus (IAV), post-infection (p.i.) model (up to d21) to examine potential longer-term effects of IAV on respiratory tissue DC subsets. In adult mice, we found differences in the kinetics and activation states of DC in the airway mucosa (AMDC) compared to those in the parenchymal lung (PLDC) compartments. A significant depletion in the percentage of AMDC was observed at day 4 p.i., associated with reversal in steady-state CD11b+:CD11b- DC subset ratios and significantly elevated CD40 and CD80 expression, that returned to baseline by d14 p.i.. In contrast, PLDC percentages and total numbers were significantly elevated at d14 p.i. and remained so until d21 p.i. Accompanying this was a reversal of CD11b+:CD11b- DC subset ratios and significant increases in both CD40 and CD80 expression. Furthermore, mice infected with IAV at 4 weeks of age showed an increase in total numbers of PLDC, and increased CD40 expression on both AMDC and PLDC, when analysed as adults at 8 weeks of age. These data suggest that the rate of recovery of DC populations following IAV infection differs in anatomical compartments of the lung, and that DC populations can remain disrupted and activated for a long period following viral clearance, possibly never fully recovering if infection occurs early in life.