Recently, cross-kingdom RNA interference, described in plants, fungi, bacteria and insects, has attracted increasing attention of scientists as a tool for protecting crops from diseases and pests.In addition, plant growth promoting bacteria, especially endophytes of the genus Bacillus, are able to activate and regulate the RNAi mechanism in plants, which makes them very promising targets for agriculture. In our work, we studied the phloem-feeding insect bird cherry-oat aphid Rhopalosiphum padi L., which, when feeding on bread wheat (Triticum aestivum L.), influenced the plant's RNAi machine to achieve its goals. In contrast, the bacterial strain Bacillus subtilis 26D promoted resistance of wheat plants to aphid by activating the RNAi mechanism and regulating the expression of nine conserved miRNAs through induction of the hormonal signaling pathways of ethylene, salicylic acid and abscisic acid, which was shown using phytohormone treatments. Different patterns of miRNA expression were found in aphid-infested plants and in plants treated with B. subtilis 26D and infested by aphids, suggesting that miRNAs play multiple roles in the plant response to phloem-feeding insects. However, these miRNAs can also enter the aphid gut along with phloem sap and affect the viability of the pest. Thus, feeding aphids with miRNA166 and miRNA408 synthesized in vitro led to an increase in pest mortality by 40 and 60%, respectively. Further comprehensive studies of the mechanisms of cross-species regulation using miRNAs may help in the development of new pesticides in modern agriculture. The study was carried out with financial support from the RSF grant 22-76-00056.