A critical transcription factor, PacC, modulates the expression of fungal pH signaling. Although PacC-mediated environmental pH has been reported to regulate the growth and pathogenicity of postharvest pathogens, the involvement of PacC in sucrose metabolism, sugar transport, and the pentose phosphate pathway (PPP) in different zones of decayed fruit remains unclear. Our work showed that the inoculation with a PePacC deletion strain of Penicillium expansum (ΔPePacC) accelerated sucrose catabolism and glucose and fructose accumulation in different zones of apple fruit. This was attributed to an increase in sucrose metabolism enzyme activities and up-regulation of the sugar transporter protein-related gene expression. Moreover, ΔPePacC inoculation increased the PPP-related enzyme activities and the levels of nicotinamide adenine dinucleotide phosphate (NADPH) and NADP+. In conclusion, PacC modulates sucrose metabolism, sugar transport, and the PPP in apple fruit by mediating dynamic changes in environmental pH, thereby enhancing fruit disease resistance.