The lungs form a highly dynamic microenvironment where airway macrophages (AMs) are key players in regulating the balance between tissue homeostasis and immune activation. Macrophage function is tightly controlled by cellular metabolism, yet it remains unclear how these processes in highly specialised tissue-resident cell populations such as AMs contribute to health and disease. Here, we show that glycolysis is a fundamental pathway that regulates lung homeostasis and responses to inhaled allergen. Employing multi-omics approaches and macrophage-specific targeting in vivo, we found that glycolytic activity in AMs was required to restrain T2 responses at homeostasis. Moreover, exposure to a variety of allergens, including the common aeroallergen house dust mite (HDM), drove glycolysis in AMs, and inhibition of glycolytic activity in AMs alleviated HDM-driven pulmonary inflammation. In line with this, we observed profound alterations in the airway metabolites specifically of HDM-sensitised patients with asthma compared to non-HDM sensitised patients or healthy controls. Finally, we found that HDM-driven glycolysis in AMs was dependent on TLR2. Thus, these data highlight a strong link between glycolysis in AMs, AM-mediated homeostatic processes and T2 inflammation in the lungs and propose a dual role for AM glycolysis in mediating lung homeostasis and inflammation. Therefore, our findings suggest that precise modulation of the optimal level of glycolysis is crucial for maintaining lung homeostasis and regulating airway inflammation and opens up new therapeutic avenues for the treatment of respiratory diseases.