A telomere-to-telomere (T2T) super-pangenome of the Citrullus genus, including all seven watermelon species, has been constructed, expanding the previously published reference genome, T2T-G42, by 399.2 Mb and 11,225 genes. This super-pangenome provides insights into watermelon evolution, domestication, and genetic diversity, revealing structural variations (SVs) and gene variants that influence traits like bitterness, sugar content, and disease resistance. Multidisease-resistant loci from wild species such as Citrullus amarus and Citrullus mucosospermus were successfully introgressed into cultivated watermelon (Citrullus lanatus), suggesting additional ancestors beyond Cordophanus in the watermelon lineage. The super-pangenome enhances understanding of watermelon genome diversity and offers comprehensive reference genomes for all Citrullus species, aiding in breeding and genetic improvement using wild relatives. Watermelon (Citrullus lanatus) is an economically important crop with low genetic diversity in cultivated accessions, limiting improvement efforts. Wild relatives, including Citrullus amarus, Citrullus mucosospermus, and others, offer valuable genetic resources for disease resistance, stress tolerance, and health-promoting compounds. The T2T super-pangenome includes 27 gap-free genomes, revealing genomic content, domestication history, and SV distribution. Comparative analysis identified SVs in C. lanatus inherited from Cordophanus and mucosospermus, indicating additional ancestors. The super-pangenome includes 27 genomes with high accuracy and continuity, containing an average of two gaps, which were filled using HiFi and ONT sequencing data. The super-pangenome includes 27 genomes with high accuracy and continuity, containing an average of two gaps, which were filled using HiFi and ONT sequencing data. Gene annotation revealed 24,698 protein-coding genes per genome, with core genes, softcore genes, dispensable genes, and private genes accounting for 42.78%, 8.80%, 45.87%, and 2.55% of total genes, respectively. SVs, which have a greater impact on genomic polymorphism and functional gene variation than SNPs, were classified into deletions, insertions, duplications, inversions, and translocations. The super-pangenome revealed narrow genetic diversity in cultivated watermelons but greater variation in wild species. SVs in wild species may contribute to trait diversity, including disease resistance, fruit sweetness, and flesh coloration. The super-pangenome also identified SVs in genes related to fruit shape, seed size, and ripening, which vary among species. Chromosomal rearrangements, such as inversions, were identified in wild and cultivated species, influencing gene expression and duplication.A telomere-to-telomere (T2T) super-pangenome of the Citrullus genus, including all seven watermelon species, has been constructed, expanding the previously published reference genome, T2T-G42, by 399.2 Mb and 11,225 genes. This super-pangenome provides insights into watermelon evolution, domestication, and genetic diversity, revealing structural variations (SVs) and gene variants that influence traits like bitterness, sugar content, and disease resistance. Multidisease-resistant loci from wild species such as Citrullus amarus and Citrullus mucosospermus were successfully introgressed into cultivated watermelon (Citrullus lanatus), suggesting additional ancestors beyond Cordophanus in the watermelon lineage. The super-pangenome enhances understanding of watermelon genome diversity and offers comprehensive reference genomes for all Citrullus species, aiding in breeding and genetic improvement using wild relatives. Watermelon (Citrullus lanatus) is an economically important crop with low genetic diversity in cultivated accessions, limiting improvement efforts. Wild relatives, including Citrullus amarus, Citrullus mucosospermus, and others, offer valuable genetic resources for disease resistance, stress tolerance, and health-promoting compounds. The T2T super-pangenome includes 27 gap-free genomes, revealing genomic content, domestication history, and SV distribution. Comparative analysis identified SVs in C. lanatus inherited from Cordophanus and mucosospermus, indicating additional ancestors. The super-pangenome includes 27 genomes with high accuracy and continuity, containing an average of two gaps, which were filled using HiFi and ONT sequencing data. The super-pangenome includes 27 genomes with high accuracy and continuity, containing an average of two gaps, which were filled using HiFi and ONT sequencing data. Gene annotation revealed 24,698 protein-coding genes per genome, with core genes, softcore genes, dispensable genes, and private genes accounting for 42.78%, 8.80%, 45.87%, and 2.55% of total genes, respectively. SVs, which have a greater impact on genomic polymorphism and functional gene variation than SNPs, were classified into deletions, insertions, duplications, inversions, and translocations. The super-pangenome revealed narrow genetic diversity in cultivated watermelons but greater variation in wild species. SVs in wild species may contribute to trait diversity, including disease resistance, fruit sweetness, and flesh coloration. The super-pangenome also identified SVs in genes related to fruit shape, seed size, and ripening, which vary among species. Chromosomal rearrangements, such as inversions, were identified in wild and cultivated species, influencing gene expression and duplication.