show Abstracthide AbstractFruit characteristics of dessert watermelon have been formed largely by human selection. Here we report an improved watermelon reference genome and a comprehensive genome variation map generated by resequencing 415 wild and cultivated accessions representing all extant species in the Citrullus genus. Genome-wide associate studies identified a number of loci associated with fruit quality traits. Population genomic analyses reveal the evolutionary history of Citrullus, suggesting a close relationship between C. lanatus and C. mucosospermus, while independent evolution in C. amarus. Our findings indicate that in watermelon different fruit size loci have been under selection during evolution, domestication and improvement. A non-bitter allele arose in the progenitor of dessert watermelon has been under selection during domestication and largely fixed in C. lanatus cultivars. Selection of flesh sweetness has been started in the progenitor of C. lanatus and continued during modern breeding through genes controlling raffinose catabolism and sugar transport from cytoplasm to vacuole. Fruit flesh coloration and sugar accumulation might have co-evolved through shared genetic components including the sugar transporter gene, ClTST2.