Fresh fruit remains highly susceptible to decay during postharvest storage and transportation, highlighting the urgent need for environmentally friendly strategies to control fungal pathogens. Some plant-derived agents stand out for their special volatile and antimicrobial properties. Here, we report the inhibitory mechanism of carvone, a natural fumigant, against pathogenic fungi. After fumigation with carvone, the colony expansion of Botrytis cinerea, Penicillium expansum and Monilinia fructicola on PDA was inhibited. Meanwhile, carvone effectively reduced gray mold incidence in stab-inoculated cherry tomatoes and grapes. As revealed by fluorescence microscopy and transmission electron microscopy, carvone compromised membrane integrity and disrupted mitochondrial ultrastructure, further abolishing normal mitochondrial potential and cell vitality. Additionally, a marked reduction in cytoplasmic ATP level was also observed. These findings collectively elucidate the mechanism by which carvone inhibits fungal pathogens on fresh fruit, while indicating that carvone may be utilized in future practice for controlling postharvest decay.