We investigated sugar metabolism in leaves and fruits of two Japanese plum (Prunus salicina Lindl.) cultivars, the climacteric Santa Rosa and its bud sport mutant the non-climacteric Sweet Miriam, during development on the tree. We previously characterized differences between the two cultivars. Here, we identified key sugar metabolic pathways. Pearson coefficient correlations of metabolomics and transcriptomic data and weighted gene co-expression network analysis (WGCNA) of RNA sequencing (RNA-Seq) data allowed the identification of 11 key sugar metabolism-associated genes: sucrose synthase, sucrose phosphate synthase, cytosolic invertase, vacuolar invertase, invertase inhibitor, α-galactosidase, β-galactosidase, galactokinase, trehalase, galactinol synthase, and raffinose synthase. These pathways were further assessed and validated through the biochemical characterization of the gene products and with metabolite analysis. Our results demonstrated the reprogramming of sugar metabolism in both leaves and fruits in the non-climacteric plum, which displayed a shift towards increased sorbitol synthesis. Climacteric and non-climacteric fruits showed differences in their UDP-galactose metabolism towards the production of galactose and raffinose, respectively. The higher content of galactinol, myo-inositol, raffinose, and trehalose in the non-climacteric fruits could improve the ability of the fruits to cope with the oxidative processes associated with fruit ripening. Overall, our results support a relationship between sugar metabolism, ethylene, and ripening behavior.