“Flavescence dorée” (FD) is a quarantine grapevine disease associated with FD phytoplasmas (FDp). In Switzerland, FD was identified in 2004 in the southernmost part of Canton Ticino (TI) and then rapidly propagated throughout the entire regional winegrowing area despite the mandatory control measures. The reported widespread distribution of gone-wild grapevines (GWGV) in TI raised the hypothesis of a potential role of GWGV as an FDp reservoir and as a habitat for FDp vectors. To test this assumption, GWGV and FDp vectors were sampled in 13 plots to attest their infection status and compare the FDp genetic profiles. The primary (Scaphoideus titanus) and best-candidate alternative (Orientus ishidae) vectors were collected throughout the season and were found in moderate to high abundance in all the study area. The infection rate of both GWGV and S. titanus followed the historical gradient of S. titanus arrival and dispersal in TI with a clear geographic distinction between the southern and northern part of TI. Interestingly, the rate measured for S. titanus was similar to that observed in highly FD-infested cultivated vineyards. Moreover, the genetic profiles of the infected GWGV and S. titanus samples were identical to those commonly observed in cultivated vineyards (map M54). Importantly, four specimens of O. ishidae were also found harboring the same genotype. This study emphasizes the importance of GWGV (and abandoned vineyards) and alternative vectors for the FD epidemics in FD-infested regions, as well as a potential origin for FD outbreaks in areas currently designated as FDp-free.