Malus Mill., a genus of temperate perennial trees with great agricultural and ecological value, has diversified through hybridization, polyploidy and environmental adaptation. Limited genomic resources for wild Malus species have hindered the understanding of their evolutionary history and genetic diversity. We sequenced and assembled 30 high-quality Malus genomes, representing 20 diploids and 10 polyploids across major evolutionary lineages and geographical regions. Phylogenomic analyses revealed ancient gene duplications and conversions, while six newly defined genome types, including an ancestral type shared by polyploid species, facilitated the detection of strong signals for extensive introgressions. The graph-based pan-genome captured shared and species-specific structural variations, facilitating the development of a molecular marker for apple scab resistance. Our pipeline for analyzing selective sweep identified a mutation in MdMYB5 having reduced cold and disease resistance during domestication. This study advances Malus genomics, uncovering genetic diversity and evolutionary insights while enhancing breeding for desirable traits.