Repeated injury can impair transitions between cellular phenotypes, potentially leading to pathological tissue repair. In recessive dystrophic epidermolysis bullosa (RDEB), collagen VII deficiency predisposes to repeated tissue injury, driving inflammation and fibrosis. Although fibroblasts are major effector cells in RDEB fibrosis, their phenotypic and molecular changes underlying disease progression remain elusive. Through cellular and in situ analyses of clinical samples and tissue from an RDEB mouse model, we disclose a phenotypic switch in dermal fibroblasts during disease progression. At early stages, fibroblasts display a contractile phenotype, whereas at later stages they transition toward a less contractile phenotype with increased production of a fibrosis-promoting extracellular matrix, indicated by high tenascin-C levels. Dysregulated epidermal growth factor receptor (EGFR) signaling through AKT appears central to this switch. At early stages, EGFR signaling and AKT support fibroblast contractility, whereas at later stages this signaling becomes intrinsically blunted, with ADAM17 implicated in the transition. The type of inflammation modulates this phenotypic switch. Thus, RDEB fibroblasts transition from a contractile to a less contractile but pro-fibrotic phenotype during disease progression. These findings suggest that reducing cellular contractility may be advantageous at earlier disease stages, whereas extracellular matrix-targeting strategies may have higher priority at later stages.