Plasmacytoid dendritic cells (pDCs) regulate immunity and promote tolerance in asthma. Notch signalling is a highly conserved pathway that regulates the immune response; however, its role in pDC‐mediated asthmatic airway inflammation is unclear. This study clarified the effects of Notch signalling on pDC‐mediated airway inflammation using murine models of ovalbumin‐sensitized allergic asthma. RBP‐J‐deficient pDCs (RBP‐J^−/− pDCs) were co‐cultured with naïve CD4⁺ T cells and supernatants and T cell subtypes were analysed. RBP‐J^−/− pDCs were intranasally transferred to the airways of ovalbumin‐sensitized recipient mice. Lung samples of all mice were subjected to tests for histopathology, cytokine profile of bronchoalveolar lavage fluid, airway hyperactivity and expression of T helper type 1 (Th1)/Th2 cells, regulatory T cells and type 2 innate lymphoid cells (ILC2s). The results showed that pDCs with and without RBP‐J deficiency significantly differed in expression levels of cluster of differentiation 83 (CD83), but not CD80, CD86 and major histocompatibility complex class II. Co‐culturing pDCs with naïve T cells revealed a poorer immunosuppressive effect of RBP‐J^−/− pDCs. This may be attributed to the lower expression levels of inducible co‐stimulator ligand and lower production of interleukin 10 in RBP‐J^−/− pDCs than in control pDCs, which impeded T cell activation and Treg suppression. RBP‐J^−/− pDCs were associated with high ILC2 expression and severe Th2 immune responses and airway inflammation. Therefore, Notch signalling is critical for pDC‐dependent immunoregulation, and RBP‐J deficiency reduces pDC‐based immunosuppression via T cell activation and Th cell differentiation. Thus, this pathway may be a therapeutic target for pDC‐based anti‐asthma immunotherapy.