Inferring the dispersal processes of vector-borne plant pathogens is a great challenge because the plausible epidemiological scenarios often involve complex spread patterns at multiple scales. European stone fruit yellows (ESFY), a disease caused by ‘ Candidatus Phytoplasma prunorum’ and disseminated via planting material and vectors belonging to the species Cacopsylla pruni , is a major threat for stone fruit production throughout Europe. The spatial genetic structure of the pathogen was investigated at multiple scales by the application of a combination of statistical approaches to a large dataset obtained through the intensive sampling of the three ecological compartments hosting the pathogen (psyllids, wild and cultivated Prunus ) in three Prunus -growing regions in France. This work revealed new haplotypes of ‘ Ca . P. prunorum’, and showed that the prevalence of the different haplotypes of this pathogen is highly uneven between all regions, and within two of them. In addition, we identified a significant clustering of similar haplotypes within a radius of at most 50 km, but not between nearby wild and cultivated Prunus . We also provide evidence that the two species of the C. pruni complex are unevenly distributed but can spread the pathogen, and that infected plants are transferred between production areas. Altogether, this work supports a main epidemiological scenario where ‘ Ca . P. prunorum’ is endemic in, and mostly acquired from, wild Prunus by immature C. pruni (of both species) who then migrate to “shelter plants” that epidemiologically connect sites less than 50 km apart by later providing infectious mature C. pruni to their “migration basins”, which differ in their haplotypic composition. We argue that such multiscale studies would be very useful for other pathosystems.