The resolution of influenza A virus (IAV) infection requires T cell-dependent immune regulation. The contribution of type I regulatory (Tr1) cells to immune regulation in the context of acute IAV infection is unknown. Here, we demonstrate that Tr1 cells enter the lung parenchyma and airways following IAV-infection, and that four distinct populations of FOXP3- IL-10+ Tr1-like cells, delineated by LAG-3 and CD49b, could be identified. RNAseq revealed that all Tr1 populations in IAV-infected lungs were enriched for co-inhibitory molecule expression and ex vivo suppression assays demonstrated that all four Tr1 populations inhibited effector T cell division, solidifying their identity as bona fide Tr1 cells. In a model of Tr1-cell deficiency, IAV infection of Il27ra-/- mice led to exacerbated weight loss and delayed recovery compared to littermate controls. Adoptive transfer of in vitro-derived polyclonal Tr1 cells into IAV-infected Il27ra-/- mice led to Tr1 cell recruitment to the lungs and significantly improved recovery from infection-induced weight loss. Overall, the findings position Tr1 cells as important mediators of immune regulation and recovery following IAV infection, and suggest potential therapeutic utility of Tr1 cells in controlling excessive inflammation following respiratory viral infection.