Fatty acids (FAs) are central to cyanobacterial physiology, shaping membrane architecture and cellular acclimatization. Because most cyanobacteria lack β-oxidation, FA fate relies on alternative pathways, including FA-derived natural products whose physiological roles remain poorly defined. Here we show that in the cyanobacterium Synechocystis salina LEGE 06099, the enzyme BrtB catalyzes the activation-independent esterification of free FAs onto the abundant secondary metabolites bartolosides, at the cell envelope, generating bartoloside fatty acid esters (B-FAs). Using stable isotope labeled FA supplementation, RNA-seq, and proteomic analyses, we find that upon exogenous FA feeding, the cellular composition of bartoloside-related metabolites change within minutes while the transcriptome and exoproteome remains unchanged. With increasing concentrations of supplied FAs, B-FA levels reach a plateau whereas bartolosides decrease and hydroxy bartolosides increase, consistent with a rapid ester hydrolysis cycle. BrtB is present at the cell envelope, and its secreted levels are not induced by FA addition, indicating a pre-positioned, envelope enzyme. Together, these results define an activation-independent FA capture pathway at the cell envelope supporting a model in which the brt system transiently sequesters free FAs to establish a steady B-FA pool while re-routing excess to membrane lipids.