Female Mediterranean fruit flies (Ceratitis capitata) oviposit in fruits, within which the larvae develop. This development is associated with rapid deterioration of the fruit, and frequently with invasion by secondary pests. Most research on the associations between medflies and microorganisms has focused on the bacteria inhabiting the digestive system of the adult fly, while the role of the fruit in mediating, amplifying or regulating the fruit fly microflora has been largely neglected. In this study, we examine the hypothesis that the host fruit plays a role in perpetuating the fly-associated bacterial community. Using direct and cultured-based approaches, we show that this community is composed in its very large majority of diazotrophic and pectinolytic Enterobacteriaceae. Our data suggest that this fly-associated enterobacterial community is vertically transmitted from the female parent to its offspring. During oviposition, bacteria are transferred to the fruit, establish and proliferate within it, causing its decay. These results show that the host fruit is indeed a central partner in the fruit fly–bacterial interaction as these transmitted bacteria are amplified by the fruit, and subsequently maintained throughout the fly's life. This enterobacterial community may contribute to the fly's nitrogen and carbon metabolism, affecting its development and ultimately, fitness.