Idiopathic pulmonary fibrosis (IPF) is characterized by persistent extracellular matrix (ECM) accumulation, yet the mechanisms governing ECM clearance remain poorly understood. In this study we investigate matricytosis, a program of ECM uptake and lysosomal degradation, and its status in disease. We show that matricytosis is highly phenotype-dependent in human macrophages and fibroblasts: disease-associated macrophages have impaired ECM internalization, while myofibroblasts demonstrate increased uptake. Inhibition studies, single-cell RNA sequencing pathway analysis and spatial transcriptomics reveal distinct uptake mechanisms for each cell type, and highlight macrophages as dominant uptake-proficient cells in both healthy and fibrotic lung tissue, while fibroblast matricytosis is linked to invasive programs prominent in IPF. Using human decellularized precision‑cut lung slices, we demonstrate that fibrotic matrix affects matricytosis and modulates cell behavior. In this work, we show that matricytosis depends on effector cell type, its phenotype and matrix environment, is dysregulated in IPF and thus, presents a potential therapeutic target.