This study investigates the role of Sox9 in vascular aging and its impact on extracellular matrix (ECM) composition and stiffness. Sox9, a transcription factor, was found to be associated with vascular senescence but not with vascular calcification. In vitro experiments showed that Sox9 expression increased in senescent vascular smooth muscle cells (VSMCs) and responded mechanosensitively, particularly on stiff matrices. Sox9 regulated ECM stiffness and organization by modulating collagen (Col) expression and reducing VSMC contractility, leading to an ECM that mimicked the senescent state. These changes in ECM promoted phenotypic modulation of VSMCs, with senescent cells plated on ECM synthesized from Sox9-depleted cells returning to a proliferative state, while proliferating cells on ECM from Sox9-expressing cells showed reduced proliferation and increased DNA damage. The study identified LH3 (procollagen-lysine, 2-oxoglutarate 5-dioxygenase 3) as a key Sox9 target and regulator of ECM stiffness, which is secreted into the ECM via extracellular vesicles (EVs). The findings highlight the crucial role of ECM structure and composition in regulating VSMC phenotype and suggest a positive feedback loop where cellular senescence and increased ECM stiffness promote Sox9 expression, further accelerating ECM modification and senescence.This study investigates the role of Sox9 in vascular aging and its impact on extracellular matrix (ECM) composition and stiffness. Sox9, a transcription factor, was found to be associated with vascular senescence but not with vascular calcification. In vitro experiments showed that Sox9 expression increased in senescent vascular smooth muscle cells (VSMCs) and responded mechanosensitively, particularly on stiff matrices. Sox9 regulated ECM stiffness and organization by modulating collagen (Col) expression and reducing VSMC contractility, leading to an ECM that mimicked the senescent state. These changes in ECM promoted phenotypic modulation of VSMCs, with senescent cells plated on ECM synthesized from Sox9-depleted cells returning to a proliferative state, while proliferating cells on ECM from Sox9-expressing cells showed reduced proliferation and increased DNA damage. The study identified LH3 (procollagen-lysine, 2-oxoglutarate 5-dioxygenase 3) as a key Sox9 target and regulator of ECM stiffness, which is secreted into the ECM via extracellular vesicles (EVs). The findings highlight the crucial role of ECM structure and composition in regulating VSMC phenotype and suggest a positive feedback loop where cellular senescence and increased ECM stiffness promote Sox9 expression, further accelerating ECM modification and senescence.