Yams are important tubers widely consumed in developing countries in various forms, mainly boiled, pounded and fried. Tuber quality is a key criterion for acceptance by the various actors in the value chain. However, the genetics of yam tuber quality has not yet been comprehensively investigated. Given this lack of knowledge, we used population genomics and candidate gene association approaches to unravel the genetic basis of the three main quality attributes of boiled yam, namely texture, starch content and colour indices. We re-sequenced the whole genome of 127 yam genotypes with different quality attributes and performed an enrichment of the already available functional genome annotation using comparative genomics. Population genomics analysis highlighted three main genetic groups and 1,053 genes under selection. We focused this work on three known quality trait-related pathways: pectin, starch content and flavonoid biosynthesis, and inventoried in the genome all the structural genes related to those pathways by comparative genomics. We improved the functional annotation of the three pathways with 48% more genes. A total of 18 candidate genes containing genetic variants significantly associated with the target traits were detected, including eight genes that were also found under selection. The texture-related candidate genes were distributed between the pectin and starch pathways. Overall, the use of comparative genomics has allowed the generation of an unprecedented genomic resource. The improved functional annotation of the yam genome is a promising predictive tool for identifying other core genes associated with any trait of interest to meet the growing need and diversified demands for yams.