The present study is the first to compare the trait-level differentiation (Qst) and the molecular-level differentiation (Fst) between Malus× domestica and Malus sieversii. A set of 115 accessions representing M.× domestica (99) and M. sieversii (16) were genotyped using the International RosBREED SNP Consortium apple 8K SNP array and phenotyped for eight fruit quality traits in a clonally replicated experiment. A set of 3521 single nucleotide polymorphisms (SNPs) with an average call rate of 98% was retained following SNP data quality filters. About 86% of the total SNPs were polymorphic in M. sieversii, while all but three SNPs were polymorphic in M. × domestica. The patterns of linkage disequilibrium were different, especially at the longer distances, between the two species. No differentiation (Fst= 0) was observed for nearly 23% of the SNPs, but about 20% of the SNPs exhibited a high genetic differentiation (Fst≥ 0.15). A highly significant (P< 0.001) genome-level Fst= 0.12 was observed between M. × domestica and M. sieversii. The average estimated Qst value was 0.20 (range 0.08–0.40), and for three of the eight studied traits (crispness, flavour intensity and fruit weight), Qst value was more than twice the estimated genome-level Fst value. A higher Qst value than Fst value for four of the eight fruit quality traits indicated differential (or directional) selection for these traits in M. × domestica. The average posterior probability of assignment of M. × domestica accessions to the M. sieversii gene pool was 11%, supporting the hypothesis of M. sieversii being one of the progenitors of the domesticated apple.