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Blueberry is well-recognized as a healthy fruit with functionality derived largely from anthocyanin and chlorogenic acid. Despite their importance, no study to date has evaluated the genetic basis of these bioactives in blueberries and their relationship with fruit quality traits. Hence, to fill this gap, a mapping population including 196 F1 individuals was phenotyped for anthocyanin and chlorogenic acid concentration and fruit quality traits (titratable acidity, pH, and total soluble solids) over 3 years and data were used for QTL mapping and correlation analysis. Total soluble solids and chlorogenic acid were positively correlated with glycosylated anthocyanin and total anthocyanin, respectively, indicating that parallel selection for these traits is possible. Across all the traits, a total of 188 QTLs were identified on chromosomes 1, 2, 4, 8, 9, 11 and 12. Notably, four major regions with overlapping major-effect QTLs were identified on chromosomes 1, 2, 4 and 8, and were responsible for acylation and glycosylation of anthocyanins in a substrate and sugar donor specific manner. Through comparative transcriptome analysis, multiple candidate genes were identified for these QTLs, including glucosyltransferases and acyltransferases. Overall, the study provides the first insights into the genetic basis controlling anthocyanins accumulation and composition, chlorogenic acid and fruit quality traits, and establishes a framework to advance genetic studies and molecular breeding for anthocyanins in blueberry.