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The genus <i>Arsenophonus</i> represents one of the most widespread clades of insect endosymbionts, including reproductive manipulators and bacteriocyte-associated primary endosymbionts. Two strains belonging to the <i>Arsenophonus</i> clade have been identified as insect-vectored plant pathogens of strawberry and sugar beet. The bacteria accumulate in the phloem of infected plants, ultimately causing leaf yellows and necrosis. These symbionts therefore represent excellent model systems to investigate the evolutionary transition from a purely insect-associated endosymbiont towards an insect-vectored phytopathogen. Using quantitative PCR and transmission electron microscopy, we demonstrate that ‘<i>Candidatus</i> Phlomobacter fragariae’, bacterial symbiont of the planthopper <i>Cixius wagneri</i> and the causative agent of Strawberry Marginal Chlorosis disease, can be transmitted from an infected strawberry plant to multiple daughter plants through stolons. Stolons are horizontally growing stems enabling the nutrient provisioning of daughter plants during their early growth phase. Our results show that <i>Phlomobacter</i> was abundant in the phloem sieve elements of stolons and was efficiently transmitted to daughter plants, which rapidly developed disease symptoms. From an evolutionary perspective, <i>Phlomobacter</i> is, therefore, not only able to survive within the plant after transmission by the insect vector, but can even be transmitted to new plant generations, independently from its ancestral insect host.