Blueberries (Vaccinium sect. Cyanococcus) are a dietary source of phenolic acids, including chlorogenic acid (CGA) and related compounds such as acetylated caffeoylquinic acid (ACQA) and caffeoylarbutin (CA). These compounds are known to be potent antioxidants with potential health benefits. While the chemistry of these compounds has been extensively studied, the genetic analysis has lagged behind. Understanding the genetic basis for traits with potential health implications may be of great use in plant breeding. By characterizing genetic variation related to fruit chemistry, breeders can make more efficient use of plant diversity to develop new cultivars with higher concentrations of these potentially beneficial compounds. Using a large interspecific F1 population, developed from a cross between the temperate V. corymbosum var. ceasariense and the subtropical V. darrowii, with 1025 individuals genotyped using genotype-by-sequencing methods, of which 289 were phenotyped for phenolic acid content, with data collected across 2019 and 2020, we have identified loci associated with phenolic acid content. Loci for the compounds clustered on the proximal arm of Vc02, suggesting that a single gene or several closely associated genes are responsible for the biosynthesis of all four tested compounds. Within this region are multiple gene models similar to hydroxycinnamoyl CoA shikimate/quinate hydroxycinnamoyltransferase (HCT) and UDP glucose:cinnamate glucosyl transferase (UGCT), genes known to be involved in the CGA biosynthesis pathway. Additional loci on Vc07 and Vc12 were associated with caffeoylarbutin content, suggesting a more complicated biosynthesis of that compound.