It remains unknown why only some allergic individuals develop asthma. Previous work has shown that allergic asthmatics (AA) recruit more pathogenic Th2 effector cells into the airway after allergen challenge compared to allergic controls (AC). We hypothesized that airway dendritic cells (DC) regulate this effector response and drive the asthma phenotype. We used segmental allergen challenge (SAC) to compare the airway response to allergen in AA (n=16) and AC (n=14). We characterized airway DC with flow cytometry and measured airway cytokines and IgE. Airway DC were sorted for RNA sequencing (n=4 per group). While AA and AC had similar baseline numbers of airway CD141+DC, AA had a higher percentage expressing the high-affinity IgE receptor (FcεRI). After SAC, CD141+DC only increased in AC. AA had higher CCL19 and CCL20 levels, and endobronchial brushings suggested mucosal accumulation of CD141+DC after SAC in AA compared to AC. AA also had higher airway levels of cytokines that promote tertiary lymphoid organ (TLO) formation and higher Th2 cytokines and IgE levels after SAC compared to AC. Airway DC in AA had 110 differentially-expressed genes in the allergen- compared to the control-challenged segment, with down-regulation of genes that promote tolerance. Our data suggest that CD141+DC in AA are primed to respond to allergen via expression of FcεRI and down-regulate tolerogenic genes in response to allergen challenge. CD141+DC may respond to DC-active chemokines by accumulating in the mucosa to serve as the nidus of TLO formation, enhancing the tissue effector response to allergen characteristic of allergic asthma.