The study generates a telomere-to-telomere (T2T) super-pangenome of *Citrullus* species, encompassing all seven species, to enhance understanding of watermelon evolution and domestication. The super-pangenome expands the previously published reference genome by adding 399.2 Mb and 11,225 genes. Comparative analysis reveals gene variants and structural variations (SVs), providing insights into the evolution and domestication of watermelon, which have enhanced traits like bitterness and sugar content while compromising disease resistance. Multidisease-resistant loci from *C. amarus* and *C. mucosospermus* were successfully introgressed into *C. lanatus*. The SVs identified in *C. lanatus* are inherited from both *cordophanus* and *C. mucosospermus*, suggesting additional ancestors beyond *cordophanus*. The study significantly improves the comprehension of watermelon genome diversity, offering comprehensive reference genomes for all *Citrullus* species and aiding in the exploration and genetic enhancement of watermelon using its wild relatives.The study generates a telomere-to-telomere (T2T) super-pangenome of *Citrullus* species, encompassing all seven species, to enhance understanding of watermelon evolution and domestication. The super-pangenome expands the previously published reference genome by adding 399.2 Mb and 11,225 genes. Comparative analysis reveals gene variants and structural variations (SVs), providing insights into the evolution and domestication of watermelon, which have enhanced traits like bitterness and sugar content while compromising disease resistance. Multidisease-resistant loci from *C. amarus* and *C. mucosospermus* were successfully introgressed into *C. lanatus*. The SVs identified in *C. lanatus* are inherited from both *cordophanus* and *C. mucosospermus*, suggesting additional ancestors beyond *cordophanus*. The study significantly improves the comprehension of watermelon genome diversity, offering comprehensive reference genomes for all *Citrullus* species and aiding in the exploration and genetic enhancement of watermelon using its wild relatives.