RelB is a member of the NF-κB family that plays a role in controlling immune and inflammatory responses. It is also essential for dendritic cell (DC) function and maturation. However, the contribution of RelB to the development of allergic airway inflammation and asthma is yet to be fully understood. Here we identify a pivotal role for RelB in the spontaneous development of allergic airway inflammation that is independent of allergen exposure. Naïve RelB deficient (RelB-/-) mice had increased total leukocytes, eosinophils, lymphocytes and neutrophils in bronchoalveolar lavage fluid (BALF); more severe peribronchial, perivascular and parenchymal inflammation, and elevated levels of Th2-associated cytokines (IL-33, TSLP, IL-25) in the lung and serum IgE, compared to heterozygote (RelB+/-) controls. RelB-/- mice had greater numbers of type 2 innate lymphoid cells (ILC2), IL-5+ and IL-13+ Th cells, myeloid dendritic cells (mDC), MHCII+ mDCs and γδ T cells in the lungs. RelB-/- mice also had increased numbers of mucus secreting cells (MSCs) and increased collagen deposition around the airways and airway epithelial thickening. Transfer of RelB+/- DCs to RelB-/- mice significantly decreased total leukocytes and eosinophils in BALF; parenchymal inflammation; Th2-associated cytokines (IL-33, TSLP, IL-25) in the lung; serum total IgE; MSCs around the airway; airway epithelial thickening; number of ILC2s, IL-5+ and IL-13+ Th cells, mDCs and γδ T cells in the lung. These findings demonstrate the importance of RelB in DCs in controlling allergic airway inflammation. Our studies identify RelB sufficient DCs as a potential therapy for allergic airway inflammation.