AbstractVesicular trafficking is an important dynamic process that facilitates intracellular transport of biological macromolecules and their release into the extracellular environment. However, little is known about whether or how plant viruses utilize intracellular vesicles to their advantage. Here, we report that southern rice black‐streaked dwarf virus (SRBSDV) enters intracellular vesicles in epithelial cells of its insect vector by engaging VAMP7 and Vti1a proteins in the soluble N‐ethylmaleimide‐sensitive factor attachment protein receptor (SNARE) complex. The major outer capsid protein P10 of SRBSDV was shown to interact with VAMP7 and Vti1a of the white‐backed planthopper and promote the fusion of vesicles into a large vesicle, which finally fused with the plasma membrane to release virions from midgut epithelial cells. Downregulation of the expression of either VAMP7 or Vti1a did not affect viral entry and accumulation in the gut, but significantly reduced viral accumulation in the haemolymph. It also did not affect virus acquisition, but significantly reduced the virus transmission efficiency to rice. Our data reveal a critical mechanism by which a plant reovirus hijacks the vesicle transport system to overcome the midgut escape barrier in vector insects and provide new insights into the role of the SNARE complex in viral transmission and the potential for developing novel strategies of viral disease control.