Staphylococcus aureus infects both humans and animals, and antimicrobial resistance, including multidrug resistance, complicates treatment of S. aureus infections. Understanding S. aureus population structure and the distribution of genetic lineages is central to understanding the biology, epidemiology, and pathogenesis of this organism. This study exploited a large, publicly available dataset of nearly 27,000 S. aureus genomes to: i) develop a core genome multilocus sequence type (cgMLST) scheme; ii) stratify hierarchical clusters based on allelic similarity thresholds; and iii) define the clusters with a life identification number (LIN) code classification system. The cgMLST scheme characterised allelic variation at 1,716 core gene loci, and 13 classification thresholds were defined, which discriminated S. aureus variants across a range of genetic similarity thresholds. LIN code lineages and clonal complexes defined by seven-locus multilocus sequence typing were highly concordant, but the LIN codes permitted a wider range of genetic discrimination among S. aureus genomes. This S. aureus cgMLST scheme and LIN code system is a high-resolution, stable genotyping tool that enables detailed genomic analyses of S. aureus.