Neofabraea vagabunda, causing bull’s eye rot, produces notable loss during cold storage of apples growing in cool humid regions. The infection initiates in the orchard, but the pathogen lives quiescently in fruit for some months before causing the symptoms of the disease. In vivo and in vitro assays were carried out to gain knowledge on the influence of fruit volatile organic compounds (VOCs) in N. vagabunda development and define volatile markers for pathogen detection, using SPME/GC‐MS, PTR‐ToF‐MS analysis and light microscopic observations. This study reports that: (i) the main VOCs of Cripps Pink apple (highly susceptible to bull’s eye rot) are degraded during the conidial germination of N. vagabunda, stimulating pathogen hyphal growth towards the host; (ii) first disease symptoms appear when fruit releases VOCs related to senescence, which also stimulate pathogen hyphal growth; (iii) VOCs typical of ripe‐senescent fruit are also emitted by infected fruit during N. vagabunda quiescence, and methanol and ethanol are the earliest markers of bull’s eye rot; and (iv) the in vitro volatile metabolism of Botrytis cinerea, Penicillium expansum and Colletotrichum fioriniae has similarities with that of N. vagabunda, but the volatile profile of each pathogen is distinguishable. Overall, this study provides novel knowledge on fruit–fungus interaction and insights for the development of tools for early disease detection in packing houses.