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Abstract Domestication of the apple was mainly driven by interspecific hybridization. In the present study, we report the haplotype-resolved genomes of the cultivated apple (Malus domesticacv. Gala) and its two major wild progenitors,M. sieversiiandM. sylvestris. Substantial variations are identified between the two haplotypes of each genome. Inference of genome ancestry identifies ~23% of the Gala genome as of hybrid origin. Deep sequencing of 91 accessions identifies selective sweeps in cultivated apples that originated from either of the two progenitors and are associated with important domestication traits. Construction and analyses of apple pan-genomes uncover thousands of new genes, with hundreds of them being selected from one of the progenitors and largely fixed in cultivated apples, revealing that introgression of new genes/alleles is a hallmark of apple domestication through hybridization. Finally, transcriptome profiles of Gala fruits at 13 developmental stages unravel ~19% of genes displaying allele-specific expression, including many associated with fruit quality.