The vascular extracellular matrix (ECM) plays a critical role in arterial mechanics, enabling large arteries to store and release energy during the cardiac cycle. In vertebrates, the elastic fiber network organized by medial smooth muscle cells is responsible for these properties. The ECM in the aortic wall is composed of structural proteins such as collagen and elastin, which provide the mechanical properties necessary for proper vascular function. As the cardiovascular system evolved, the ECM composition changed to accommodate increased pulse pressure and more complex vascular demands. The mechanical properties of the vessel wall are closely related to physiological blood pressure across species, and a universal elastic modulus governs ECM deposition during vascular development. This review discusses the structural ECM proteins in the vertebrate aortic wall and how their composition has evolved. It also explores mechanical models that can aid in designing better tissue-engineered vessels and testing clinical treatments. The review highlights the importance of the vascular ECM in providing structural and mechanical support, as well as instructive signals that guide vascular cell phenotypes. The vascular ECM is essential for vascular development, and its composition changes during embryogenesis, vessel maturation, and injury response. The review also discusses the structure and function of the arterial wall, including the tunica intima, media, and adventitia, and the role of vascular smooth muscle cells in vascular development. The review covers the evolution of the vascular ECM, the role of elastin and microfibrils in elastic fiber formation, and the functions of various ECM proteins such as fibrillin, microfibril-associated glycoproteins, fibulins, and lysyl oxidase. The review also discusses the expression patterns of these proteins during vascular development and their roles in maintaining vascular structure and function. The review concludes with the importance of the vascular ECM in vascular development and the need for further research to understand its complex functions.The vascular extracellular matrix (ECM) plays a critical role in arterial mechanics, enabling large arteries to store and release energy during the cardiac cycle. In vertebrates, the elastic fiber network organized by medial smooth muscle cells is responsible for these properties. The ECM in the aortic wall is composed of structural proteins such as collagen and elastin, which provide the mechanical properties necessary for proper vascular function. As the cardiovascular system evolved, the ECM composition changed to accommodate increased pulse pressure and more complex vascular demands. The mechanical properties of the vessel wall are closely related to physiological blood pressure across species, and a universal elastic modulus governs ECM deposition during vascular development. This review discusses the structural ECM proteins in the vertebrate aortic wall and how their composition has evolved. It also explores mechanical models that can aid in designing better tissue-engineered vessels and testing clinical treatments. The review highlights the importance of the vascular ECM in providing structural and mechanical support, as well as instructive signals that guide vascular cell phenotypes. The vascular ECM is essential for vascular development, and its composition changes during embryogenesis, vessel maturation, and injury response. The review also discusses the structure and function of the arterial wall, including the tunica intima, media, and adventitia, and the role of vascular smooth muscle cells in vascular development. The review covers the evolution of the vascular ECM, the role of elastin and microfibrils in elastic fiber formation, and the functions of various ECM proteins such as fibrillin, microfibril-associated glycoproteins, fibulins, and lysyl oxidase. The review also discusses the expression patterns of these proteins during vascular development and their roles in maintaining vascular structure and function. The review concludes with the importance of the vascular ECM in vascular development and the need for further research to understand its complex functions.