Intramuscular fibrosis impairs muscle function in patients with Duchenne muscular dystrophy (DMD), reducing physical activity and posing a fatal risk when it affects the heart muscle. Although fibro-adipogenic progenitor cells (FAPs) have recently been identified as key contributors to intramuscular fibrosis, their role in muscular dystrophy remains incompletely understood. To identify the characteristics of FAPs in DMD, we first generated FAP reporter DMD mice by crossing GFP reporter mice with D2-mdx mice (and DBA2/J mice as control) for 6 generations. and DBA2/J mice for PDGFRa, a FAP-specific marker. Two groups of 12-month-old male mice—PDGFRα reporter DBA2/J (PRDBA) and PDGFRα reporter D2-mdx (PRD2) were sacrificed, and their tibialis anterior (TA) muscles, diaphragm muscles, and hearts were collected for histology (n = 6 in each) and FAPs single-cell RNA sequencing (scRNAseq) analysis (n = 3 in each). In all tissue types, both the fibrotic area and the number of PDGFRα+ cells were significantly higher in PRD2 mice compared to PRDBA mice. Cell population distribution plots from FAP scRNAseq revealed an increased proportion of pre-fibrogenic FAPs, identified by the gene CD55, in all groups with DMD compared to control (CTL) [TA: CTL (31.2%) vs DMD (41.4%), Diaphragm: CTL (10.9%) vs DMD (12.7%), Heart: CTL (16.0%) vs DMD (22.2%)]. Pseudotime clustering analysis supported enhanced fibrogenic progression from progenitor cells in DMD. These results indicate increased FAP cell population and fibrogenesis in both skeletal and cardiac muscles due to dystrophin deficiency, leading to fibrosis in both skeletal and cardiac muscles. Inhibiting FAP proliferation and fibrogenesis may represent a promising therapeutic approach for treating muscle fibrosis in DMD.