Staphylococcus aureus is a highly contagious mastitis-causing pathogen infecting dairy cattle worldwide. Previous studies have shown the presence of different genotypes (GT) on farms. In Switzerland, Staph. aureus genotype B (GTB) is contagious, whereas GTC and other genotypes cause sporadic, noncontagious mastitis. In this study, we evaluated the epidemiological properties of Staph. aureus, together with its genotypes and spa types, on Swiss dairy farms. A total of 21 dairy farms were sampled throughout Switzerland; 10 farms were positive for the contagious Staph. aureus GTB and 11 farms were negative for GTB. Samples were taken from milk, body surfaces of dairy cattle and other animals, milkers, milking equipment, and environmental sites (e.g., parlor, washing room, stall floor, manger, and bedding). The epidemiology of Staph. aureus depended markedly on the genotype. Staphylococcus aureus GTB was associated with mammary gland, intramammary infections (IMI), and milking clusters, whereas GTC and other genotypes were related to cow and other animal surfaces and occasionally to environment. Genotype C was by far the most common subtype in cattle and was found on GTB-negative and GTB-positive farms. Each farm had a predominant genotype, such as GTB, GTC, GTA, or GTF, but a few farms were almost free from Staph. aureus. The genotypes and spa types of Staph. aureus detected in the noses of milkers clearly differed from those found in dairy cattle, other animals, milking equipment, and the environment. Exceptions were GTS (spa type t034) and GTF (t899), which crossed the species barrier. In most cases, however, the species barrier was maintained because Staph. aureus is adapted to a particular host and even to particular body sites. As biological properties differ among the genotypes, new guidelines to prevent IMI caused by different genotypes were established: classical measures to prevent IMI caused by contagious pathogens still hold for GTB but not for Staph. aureus genotypes that are opportunistic colonizers of bovine skin (e.g., GTC and GTA). For those genotypes, protection of the skin from minor lesions and wounds, particularly on the hocks, is essential.