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Severe peritoneal fibrosis with encapsulation or encapsulating peritoneal sclerosis is devastating and life\u2010threatening. Although submesothelial fibroblasts as the major precursor of scar\u2010producing myofibroblasts in animal models and M2 macrophage (M\u03d5)\u2010derived chemokines in peritoneal effluents of patients before diagnosis of encapsulating peritoneal sclerosis have been identified, attenuation of peritoneal fibrosis is an unmet medical need partly because the mechanism for cross talk between M\u03d5s and fibroblasts remains unclear. We use a sodium hypochlorite\u2010induced mouse model akin to clinical encapsulated peritoneal sclerosis to study how the peritoneal M\u03d5s activate fibroblasts and fibrosis. Sodium hypochlorite induces the disappearance of CD11b<jats:sup>high<\/jats:sup>F4\/80<jats:sup>high<\/jats:sup> resident M\u03d5s but accumulation of CD11b<jats:sup>int<\/jats:sup>F4\/80<jats:sup>int<\/jats:sup> inflammatory M\u03d5s (InfM\u03d5s) through recruiting blood monocytes and activating local cell proliferation. InfM\u03d5s switch to express chemokine (C\u2010C motif) ligand 17 (CCL17), CCL22, and arginase\u20101 from day 2 after hypochlorite injury. More than 75% of InfM\u03d5s undergo genetic recombination by <jats:italic>Csf1r<\/jats:italic>\u2010driven Cre recombinase, providing the possibility to reduce myofibroblasts and fibrosis by diphtheria toxin\u2010induced M\u03d5 ablation from day 2 after injury. Furthermore, administration of antibody against CCL17 can reduce M\u03d5s, myofibroblasts, fibrosis, and improve peritoneal function after injury. Mechanistically, CCL17 stimulates migration and collagen production of submesothelial fibroblasts in culture. By breeding mice that are induced to express red fluorescent protein in M\u03d5s and green fluorescence protein (GFP) in Col1a1\u2010expressing cells, we confirmed that M\u03d5s do not produce collagen in peritoneum before and after injury. However, small numbers of fibrocytes are found in fibrotic peritoneum of chimeric mice with bone marrow from Col1a1\u2010GFP reporter mice, but they do not contribute to myofibroblasts. These data demonstrate that InfM\u03d5s switch to pro\u2010fibrotic phenotype and activate peritoneal fibroblasts through CCL17 after injury. CCL17 blockade in patients with peritoneal fibrosis may provide a novel therapy. \u00a9 2019 Pathological Society of Great Britain and Ireland. 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