$Staphylococcus\; argenteus$ is a newly named species previously described as a divergent lineage of Staphylococcus aureus that has recently been shown to have a global distribution. Despite growing evidence of the clinical importance of this species, knowledge about its population epidemiology and genomic architecture is limited. We used whole-genome sequencing to evaluate and compare $S.\; aureus$ (n 251) and $S.\; argenteus$ (n 68) isolates from adults with staphylococcal sepsis at several hospitals in northeastern Thailand between 2006 and 2013. The majority (82%) of the $S.\; argenteus$ isolates were of multilocus sequence type 2250 (ST2250). $S.\; aureus$ was more diverse, although 43% of the isolates belonged to ST121. Bayesian analysis suggested an $S.\; argenteus$ ST2250 substitution rate of 4.66 (95% confidence interval [CI], 3.12 to 6.38) mutations per genome per year, which was comparable to the $S.\; aureus$ ST121 substitution rate of 4.07 (95% CI, 2.61 to 5.55). $S.\; argenteus$ ST2250 emerged in Thailand an estimated 15 years ago, which contrasts with the $S.\; aureus$ ST1, ST88, and ST121 clades that emerged around 100 to 150 years ago. Comparison of $S.\; argenteus$ ST2250 genomes from Thailand and a global collection indicated a single introduction into Thailand, followed by transmission to local and more distant countries in Southeast Asia and further afield. $S.\; argenteus$ and $S.\; aureus$ shared around half of their core gene repertoire, indicating a high level of divergence and providing strong support for their classification as separate species. Several gene clusters were present in ST2250 isolates but absent from the other $S.\; argenteus$ and $S.\; aureus$ study isolates. These included multiple exotoxins and antibiotic resistance genes that have been linked previously with livestock-associated $S.\; aureus$, consistent with a livestock reservoir for $S.\; argenteus$. These genes appeared to be associated with plasmids and mobile genetic elements and may have contributed to the biological success of ST2250.