Plum pox virus (PPV) is one of the most economically important plant viruses. PPV M strain (PPV-M) was first isolated in Japan in 2016. The infection cycle of PPV by vector aphids remains unknown in Japan. Here, we present a seasonal model describing the infection cycle of PPV-M in Japanese apricot orchards. First, by mechanically inoculating twelve herbaceous species belonging to Asteraceae (alternatively Compositae) in orchards with PPV-M, we found that all were susceptible to infection. Of those, Hemisteptia lyrata showed high infection rates on the upper leaves. Second, a subsequent survey of multiple aphid species parasitizing H. lyrate showed a seasonal infection cycle in which A. fabae solanella likely transmitted PPV-M from Japanese apricot leaves to H. lyrata in the spring. Then, A. spiraecola, an efficient PPV vector known to shift between hosts in summer and autumn, transmitted the disease to healthy Japanese apricot seedlings from PPV-M infected H. lyrate in autumn. We propose that PPV-M in Japanese apricot follows a seasonal and multimodal infection cycle involving an intermediate host (Asteracease) and two aphid species.