Staphylococcus aureus is a widespread commensal and opportunistic pathogen capable of colonising diverse host species, including humans and animals. While zoonotic transmission between livestock and humans has been well documented, comparatively little is known about the role of companion animals in the ecology and transmission of S. aureus.   We combined genomic and epidemiological approaches to investigate S. aureus carriage and persistence among domestic cats, cat shelter populations, and their human contacts. Comparative whole-genome analysis of isolates from cohabiting humans and cats revealed, for the first time, direct genetic evidence of within-household S. aureus transmission. Human and feline isolates from the same households were often separated by only a few single-nucleotide polymorphisms, indicating very recent transmission events and suggesting that close contact facilitates bacterial exchange between species.   In cat shelters, longitudinal sampling identified the persistence of identical or near-identical S. aureus genotypes across multiple animals and environmental samples over several months. This pattern suggests stable colonisation and repeated reintroduction within shared environments, supporting the existence of ecological niches that sustain S. aureus circulation independent of new external introductions.   Together, these findings demonstrate that S. aureus can both transmit between humans and cats within households and persist over time within multi-animal environments. These results highlight the importance of companion animals and their environments in the broader One Health context of S. aureus ecology and transmission.