The present study is the first to compare the trait-level differentiation (Q st) and the molecular-level differentiation (F st) 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 (F st= 0) was observed for nearly 23% of the SNPs, but about 20% of the SNPs exhibited a high genetic differentiation (F st≥ 0.15). A highly significant (P< 0.001) genome-level F st= 0.12 was observed between M. × domestica and M. sieversii. The average estimated Q st value was 0.20 (range 0.08–0.40), and for three of the eight studied traits (crispness, flavour intensity and fruit weight), Q st value was more than twice the estimated genome-level F st value. A higher Q st value than F st 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.