Sox9 accelerates vascular aging by regulating extracellular matrix (ECM) composition and stiffness. This study shows that Sox9 is upregulated in vascular aging and is associated with cellular senescence. In vitro, Sox9 expression increases in senescent vascular smooth muscle cells (VSMCs) and on stiff matrices, leading to changes in ECM stiffness and organization. These changes mimic features of senescent cells, promoting phenotypic modulation of VSMCs. Senescent cells plated on ECM from Sox9-depleted cells return to a proliferative state, while proliferating cells on a matrix produced by Sox9-expressing cells show reduced proliferation and increased DNA damage, resembling senescent cells. LH3, a Sox9 target, is packaged into extracellular vesicles and promotes ECM stiffness. These findings highlight the crucial role of ECM structure and composition in regulating VSMC phenotype. A positive feedback cycle exists, where cellular senescence and increased ECM stiffness promote Sox9 expression, which further drives ECM modifications, accelerating stiffening and senescence. Sox9 regulates ECM stiffness through activation of LH3, a key regulator of ECM stiffness. The study also identifies the role of extracellular vesicles in promoting ECM stiffness. These findings suggest that Sox9 plays a key role in vascular aging by regulating ECM composition and stiffness, and that LH3 and extracellular vesicles are important drivers of ECM stiffening with age. The study underscores the importance of ECM composition in regulating VSMC aging and highlights the need for further investigation into the regulatory mechanisms underlying these processes.Sox9 accelerates vascular aging by regulating extracellular matrix (ECM) composition and stiffness. This study shows that Sox9 is upregulated in vascular aging and is associated with cellular senescence. In vitro, Sox9 expression increases in senescent vascular smooth muscle cells (VSMCs) and on stiff matrices, leading to changes in ECM stiffness and organization. These changes mimic features of senescent cells, promoting phenotypic modulation of VSMCs. Senescent cells plated on ECM from Sox9-depleted cells return to a proliferative state, while proliferating cells on a matrix produced by Sox9-expressing cells show reduced proliferation and increased DNA damage, resembling senescent cells. LH3, a Sox9 target, is packaged into extracellular vesicles and promotes ECM stiffness. These findings highlight the crucial role of ECM structure and composition in regulating VSMC phenotype. A positive feedback cycle exists, where cellular senescence and increased ECM stiffness promote Sox9 expression, which further drives ECM modifications, accelerating stiffening and senescence. Sox9 regulates ECM stiffness through activation of LH3, a key regulator of ECM stiffness. The study also identifies the role of extracellular vesicles in promoting ECM stiffness. These findings suggest that Sox9 plays a key role in vascular aging by regulating ECM composition and stiffness, and that LH3 and extracellular vesicles are important drivers of ECM stiffening with age. The study underscores the importance of ECM composition in regulating VSMC aging and highlights the need for further investigation into the regulatory mechanisms underlying these processes.