Background: Asthmatic airway remodeling is characterized by goblet cell hyperplasia, angiogenesis, smooth muscle hypertrophy and sub-epithelial fibrosis. Objective: This study evaluated whether acquired changes in fibroblast phenotype could contribute to this remodeling. Methods: Airway and parenchymal fibroblasts from control or chronically ovalbumin-sensitized and challenged "asthmatic" mice were assessed for several functions related to repair and remodeling ± exogenous transforming growth factor-₁(TGF-₁) and gene expression profiles were evaluated. Results: All OVA challenged mouse fibroblasts demonstrated augmented gel contraction (p<0.05) and chemotaxis (p<0.05), increased TGF-1 (p<0.05), fibronectin (p<0.05), and vascular endothelial growth factor (p<0.05) release and expressed more -smooth muscle actin (p < 0.05). TGF-₁ stimulated both control and asthmatic fibroblasts, which retained all differences from control fibroblasts for all features(p <0.05, all comparisons). Parenchymal fibroblasts proliferated more rapidly (p<0.05), while airway fibroblasts proliferated similarly compared with control fibroblasts (p=0.25). Conclusion: Thus, in this animal model, OVA challenged mouse fibroblasts acquire a distinct phenotype that differs from control fibroblasts. Clinical Implication: The augmented profibrotic activity and mediator release of asthmatic fibroblasts could contribute to airway remodeling in asthma. Capsule summary: Lung fibroblasts cultured from ovalbumin sensitized mice manifest persistent differences in vitro in phenotypes related to repair and remodeling. This suggests that acquired alterations of fibroblast repair phenotypes can contribute to the pathogenesis of asthma.