Staphylococcus aureus is a widespread opportunistic pathogen to humans and animals. Of its genome, 20 to 25% varies between strains and consists of phages, pathogenicity islands, transposons, and genomic islands. S. aureus harbors up to three genomic islands, vSaα, vSaβ, and vSaγ. The vSaβ region of S. aureus can encode a number of virulence-associated factors, such as serine proteases, leukocidins, enterotoxins, bacteriocins, or a hyaluronate lyase. In this study, the vSaβ regions of 103 clinically relevant S. aureus strains were characterized in silico and compared to the three predefined vSaβ types. We here suggest a superordinate system of 15 different vSaβ types, of which 12 were newly defined. Each vSaβ type has a distinct structure with a distinct set of genes, which are both highly conserved. Between the different types, gene content and composition vary substantially. Based on our data, a strain’s vSaβ type is strongly coupled with its clonal complex, suggesting that vSaβ was acquired in an ancestral S. aureus strain, arguably by phage mediation, before differentiation into clonal complexes. In addition, we addressed the issue of ambiguous nomenclature in the serine protease gene cluster and propose a novel, phylogeny-based nomenclature of the cluster contained in the vSaβ region.