Evolution of the spread strategies of plant pathogens may be described using the vector manipulation hypothesis (VMH), which posits that pathogens can enhance their transmission to new host plants through their effects on mobile vectors. Barley yellow dwarf virus (BYDV) transmitted by aphid vectors in wheat has become increasingly important as a model pathosystem. However, the role of alate aphids in virus spread has attracted little attention although the migratory morph is a key vector for the long-distance dispersal of plant pathogens. Herein, we first examined the selection preferences of alate or aptera morphs of the vector Schizaphis graminum for healthy/mock-inoculated/BYDV-infected wheat plants and then identified possible volatile components that influenced alate S. graminum selection behavior. The results showed that noninfective S. graminum (either alate or aptera) mainly tended to select BYDV-infected wheat while infective S. graminum (only aptera) preferentially selected noninfected wheat. In addition, we found that the BYDV-infected plants showed significant differences in the content and quantity of volatiles compared with healthy or mock-inoculated wheat plants and that the increased volatiles (trans-2-hexen-1-al or decanal) released by BYDV-infected plants may play a critical role in attracting noninfective alate aphids in a concentration-dependent manner. These findings describe a novel mechanism by which the volatile profiles released by virus-infected plants may influence alate aphid colonization preference, providing further or new evidences for the VMH. This study extends our knowledge base on plant virus transmission to new host plants with potential ramifications for the integrated management of both the vector and disease.