AbstractFruit characteristics of sweet watermelon are largely the result of human selection. Here we report an improved watermelon reference genome and whole-genome resequencing of 414 accessions representing all extant species in theCitrullusgenus. Population genomic analyses reveal the evolutionary history ofCitrullus, suggesting independent evolutions inCitrullus amarusand the lineage containingCitrullus lanatusandCitrullus mucosospermus. Our findings indicate that different loci affecting watermelon fruit size have been under selection during speciation, domestication and improvement. A non-bitter allele, arising in the progenitor of sweet watermelon, is largely fixed inC. lanatus. Selection for flesh sweetness started in the progenitor ofC. lanatusand continues through modern breeding on loci controlling raffinose catabolism and sugar transport. Fruit flesh coloration and sugar accumulation might have co-evolved through shared genetic components including a sugar transporter gene. This study provides valuable genomic resources and sheds light on watermelon speciation and breeding history.