Allele dosage plays a key role in the phenotypic variation of polyploids. Here we present a genome-wide variation map of hexaploid sweet potato that captures allele dosage information, constructed from deep sequencing of 294 hexaploid accessions. Genome-wide association studies identified quantitative trait loci with dosage effects on 23 agronomic traits. Our analyses reveal that sweet potato breeding has progressively increased the dosage of favourable alleles to enhance trait performance. Notably, the Mesoamerican gene pool has evolved towards higher dosages of favourable alleles at multiple loci, which have been increasingly introgressed into modern Chinese cultivars. We substantiated the breeding-driven dosage accumulation through transgenic validation of IbEXPA4, an expansin gene influencing tuberous root weight. In addition, we explored causative sequence variations that alter the expression of the Orange gene, which regulates flesh colour. Our findings illuminate the breeding history of sweet potato and establish a foundation for leveraging allele dosages in polyploid breeding practices.