Dietary anthocyanins are important health-promoting antioxidants that make a major contribution to the quality of fruits. It is intriguing that most tomato cultivars do not produce anthocyanins in fruit. However, the purple tomato variety Indigo Rose, which combines the dominant Aft locus and the recessive atv locus from wild tomato species, exhibits light-dependent anthocyanin accumulation in the skin. Here, we report that whereas Aft encodes a functional allele of an anthocyanin activator named SlAN2-like, atv encodes a non-functional allele of the anthocyanin repressor SlMYBATV. The expression of SlAN2-like is responsive to light and a functional SlAN2-like can activate both anthocyanin biosynthetic genes and their regulatory genes, suggesting that SlAN2-like acts as a master regulator and plays a critical role for the activation of anthocyanin biosynthesis. Our results reveal that cultivated tomatoes contain a non-functional allele of this master regulator and therefore fail to produce anthocyanins. Indeed, expression of a functional SlAN2-like in a tomato cultivar led to the activation of the entire anthocyanin biosynthesis pathway and high levels of anthocyanin accumulation in both peel and flesh. Our study exemplifies that efficient engineering of complex metabolic pathways could be achieved through tissue-specific expression of master transcriptional regulators.