Interspecific hybridization may trigger species radiation by creating allele combinations and traits. Cultivated potato and its 107 wild relatives from the Petota lineage all share the distinctive trait of underground tubers, but the underlying mechanisms for tuberization and its relationship to extensive species diversification remain unclear. Through analyses of 128 genomes, including 88 haplotype-resolved genomes, we revealed that Petota is of ancient hybrid origin, with all members exhibiting stable mixed genomic ancestry, derived from the Etuberosum and Tomato lineages ca. 8-9 million years ago. Our functional experiments further validated the crucial roles of parental genes in tuberization, indicating that interspecific hybridization is a key driver of this innovative trait. This trait, along with the sorting and recombination of hybridization-derived polymorphisms, likely triggered the explosive species diversification of Petota by enabling occupation of broader ecological niches. These findings highlight how ancient hybridization fosters key innovation and drives subsequent species radiation.