Valsa canker (VC), caused by the fungus Valsa mali, represents a significant threat to Malus plants, including both domestic apple and crabapple varieties. The identification of genes that confer resistance or susceptibility is a pivotal step in the breeding of new cultivars and the sustainable development of Malus. In this study, we present chromosome-level and near-gapless genome assemblies of two ornamental crabapple cultivars, M. ‘Prairifire’ and M. ‘Hopa’, which exhibit contrasting resistance and susceptibility to VC. Through transcriptomic analysis and quantitative real-time PCR (qRT-PCR) validation, we identified eight genes that are up-regulated during infection of M. ‘Prairifire’ by V. mali. These genes are involved in encoding various proteins, including a Yippee-like protein, secoisolariciresinol dehydrogenase, a valine-glutamine (VQ) motif-containing protein, a 23 kDa jasmonate-induced protein, a kinase domain-containing protein, a Tobacco Mosaic Virus (TMV) resistance protein, a calmodulin-related protein, and a detoxification protein. The results provide valuable genomic resources for a comprehensive investigation into the genetic basis of resistance to VC and provide a basis for the future molecular breeding of Malus.