Background: Macrophages, as one of the most abundant immune cells in the lung, has drawn great attention in allergic asthma. Currently, most studies emphasize on M2 polarization bias. However, the function of macrophages in allergic asthma is still controversial. IL-9 contributes to the development and pathogenesis of allergic airway inflammation. We sought to investigate the IL-9-producing macrophage subset and its role in allergic asthma. Methods: The model of OVA-induced allergic airway inflammation was employed to evaluate IL-9 production in macrophages of lung tissues. We used 22 cytokines or stimuli to screen for IL-9-producing mouse macrophage subset in vitro, and real-time PCR, flow cytometry, ELISA, immunofluorescence and RNA-seq to explore the M(IL-33+IL-2) subset. Mice with Lyz-IL-33 receptor conditional knockout and adoptive transfer M(IL-33+IL-2) were used to characterize the potential roles of M(IL-33+IL-2) in allergic airway inflammation. Results: We identified a unique pathogenic IL-9-producing macrophage subset in OVA-induced allergic airway inflammation. We found that only IL-33 significantly induced IL-9 production in mouse macrophages, and IL-2 collaborated with IL-33 to promote macrophages to produce IL-9, referred to as M(IL-33+IL-2). Importantly, human monocyte-derived macrophages produced IL-9 after IL-33 and IL-2 stimulation. Using mice with Lyz-IL-33 receptor conditional knockout and adoptive transfer of M(IL-33+IL-2), we found that M(IL-33+IL-2) significantly promoted pathogenesis in OVA-induced allergic airway inflammation. M(IL-33+IL-2) subset has a distinctive gene expression profile with high expression of cytokines and M(IL-33+IL2) polarization is dependent on JAK2-STAT3-IRF1 pathway. Conclusions: The identification of M(IL-33+IL-2) subset extends the diversity and heterogeneity of macrophage subsets, and may offer novel therapeutic strategies for treatment of allergic inflammation.