While native to ~30% of the population, S. aureus is labeled a serious health threat by the CDC due to its infectious prevalence and growing antibiotic resistance. While genetic factors have been linked with antibiotic resistance, recent antibiotics such as daptomycin directly target the bacteria’s lipid membrane, yet the impact of physiological and morphological changes to the bacterial membrane on drug resistance is critically understudied. Via pathways such as the fatty acid kinase pathway exogenous free fatty acids are able to be directly incorporated into the S. aureus lipidome changing the membranes physiology, yet the vast majority of fatty acids are esterified within the phospho- and glycolipid population of the body. However, S. aureus has been found to secrete a lipase known as glycerol ester hydrolase, Geh, able to selectively hydrolyze diacyl lipids both liberating a free fatty acid drastically changing both the bacterial and host lipidome. Given this knowledge, we employed a two-fold lipidomic study jointly investigating the changing bacterial and environmental lipidome when S. aureus is exposed to biologically relevant mixture of exogenous phospholipid. These findings provide a critical next step in understanding the complex dynamics within the infectious environment.