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Volatile fatty acids (VFAs) have emerged as promising alternative substrates to replace sugars (such as glucose) for microbial production, which can help reduce production costs. Moreover, VFAs can be sustainably produced through anaerobic fermentation (AF) of organic waste streams, revalorizing these by-products and thus contributing to the transition toward a circular bio-based economy. However, finding microorganisms able to tolerate and consume VFAs is a crucial need to achieve this goal. This study assesses, for the first time, the ability of the halotolerant and oleaginous non-conventional yeast Debaryomyces hansenii (D. hansenii) to metabolize VFAs as the sole carbon and energy source, using different total VFAs concentrations and acid profiles in synthetic media as well as microalgae VFAs-rich digestates. D. hansenii was able to grow with up to 15 g/L of total VFAs and metabolize all of them when acetic acid was the main acid present in the medium. An improved growth of the yeast was observed when using an organic VFAs-rich digestate as a feedstock derived from the AF of microalgae biomass, compared to growth in synthetic media. In this case, a biomass yield of 0.43 g/g was achieved. Finally, the capability of D. hansenii to produce and accumulate lipids from VFAs was assessed, showing that when the C:N ratio of the medium was increased to 200, the yeast accumulated up to 20.87% w/w of lipids, being oleic, palmitic, and linoleic acids the primary fatty acids produced. Interestingly, the odd-chain fatty acid C17 was also detected. Our study shows the potential of D. hansenii for bioconversion of VFAs, particularly from organic digestates, into industrially high-value compounds such as lipids. This particular yeast exhibits a preference for acetic acid and the ability to metabolize a wide range of VFAs when this acid is supplied in higher concentrations than the others. Our research moreover highlights the importance of C:N ratio and VFA composition for lipid accumulation in Debaryomyces and furthermore provides a foundation for further exploration of D. hansenii as a suitable candidate for sustainable bioproduction of microbial oils.