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Wild loquats (Eriobotrya japonica Lindl.) provide remarkable genetic resources for studying domestication and breeding improved varieties. Herein, we generate the first high-quality chromosome-level genome assembly of wild loquat, with the 45,791 predicted protein-coding genes. Analysis of comparative genomics indicated that loquat shared a common ancestor with apple and pear, and a recent whole-genome duplication event occurred in loquat prior to its divergence. Genome re-sequencing showed that the loquat germplasms were distinctly classified into wild and cultivated groups, and the commercial cultivars experienced allelic admixture. Compared with the cultivated loquats, the wild loquat genome showed very few selected genomic regions and had higher levels of genetic diversity. However, whole-genome scans of selective sweeps were mainly related to fruit quality, size, and flesh color during the domestication process. Large-scale transcriptome and metabolome analyses were further performed to identify the differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) in the wild and cultivated loquats, at various fruit development stages. Unlike that in wild loquat, the key DEGs and DAMs involved in carbohydrate metabolism, plant hormone signal transduction, flavonoid biosynthesis, and carotenoid biosynthesis were significantly regulated in cultivated loquats during fruit development. These high-quality reference genome, re-sequencing, and large-scale transcriptome/metabolome data provide valuable resources for elucidating fruit domestication and molecular breeding in loquat.