Given the central role of livestock in understanding the genomic epidemiology of S. aureus, the present study systematically reviewed and synthesized data on the nasal S. aureus carriage, resistance patterns to critical antimicrobial agents, virulence factors and genetic lineages among healthy livestock. Bibliographical databases were searched for published studies from May 2003 to May 2022 on nasal S. aureus carriage, their phenotypic and genetic characteristics among healthy pigs (A), sheep and goats (B), cattle (C), poultry (D), camels (E) and buffaloes (F). Special focus was given to the prevalence of nasal MRSA, MRSA-CC398, MRSA-CC9, mecC-MRSA, MSSA-CC398, and resistance to linezolid (LZD^R), chloramphenicol (CLO^R) and tetracycline (TET^R) in S. aureus isolates. Of the 5492 studies identified, 146 comprised groups A(83)/B(18)/C(33)/D(4)/E(5)/F(3), and were found eligible. The overall pooled nasal prevalence of MRSA in healthy livestock was 13.8% (95% CI: 13.5–14.1) among a pooled 48,154 livestock population. Specifically, the pooled prevalence in groups A to F were: 16.0% (95% CI: 15.6–16.4), 3.7% (95% CI: 2.9–4.6), 13.6% (95% CI: 12.8–14.4), 5.8% (95% CI: 5.1–6.5), 7.1% (95% CI: 6.1–10.7), and 2.8% (95% CI: 1.5–4.8), respectively. These values varied considerably by continent. Varied pooled prevalences of CC398 lineage with respect to MRSA isolates were obtained, with the highest from pigs and cattle (>70%). Moreover, other classical animal-adapted MRSA as well as MSSA-CC398-t1928 were reported. TET^R-MSSA was lowest in cattle (18.9%) and highest in pigs (80.7%). LZD^R-S. aureus was reported in 8 studies (mediated by optrA and cfr), mainly in pigs (n = 4), while CLO^R-S. aureus was reported in 32 studies. The virulence genes luk-S/F-PV, tst, etd, sea, see were sparsely reported, and only in non-CC398-MRSA lineages. Certain S. aureus clones and critical AMR appeared to have predominance in some livestock, as in the case of pigs that are high nasal carriers of MRSA-CC398 and -CC9, and MSSA-CC398. These findings highlight the need for adequate prevention against the transmission of zoonotic S. aureus lineages to humans.