The tritrophic interactions among plant virus, host plants, and insect vectors directly influence the natural ecosystem, which, in turn, has tremendous practical implications in the sustainable pest control strategies. Cucumber mosaic virus (CMV), transmitted by aphids in a non-persistent manner, causes severe damage in diverse crops worldwide. There is a wealth of information on the initial round of interactions within this tritrophic system. However, knowledge on the subsequent round of interactions is very limited. In this research, we focused on their interactions among Nicotiana tabacum cv. Samsum plants, CMV, and green peach aphids, Myzus persicae specifically after the initial round of aphid feeding on CMV-infected plants. Our results show that initial aphid feeding on CMV-infected plants reduces the fitness of the subsequent aphids. The reproduction capacity, longevity, and survival rate of M. persicae are reduced on CMV-infected plants, previously foraged by M. persicae. Furthermore, the initial aphid feeding on CMV-infected plants induce gene expression involved in the salicylic acid (SA) signaling pathway and suppresses the expression of downstream genes associated with jasmonic acid (JA) signaling pathway. Besides, plant chlorophyll content and nitrogen source are reduced on those CMV-infected plants, previously foraged by aphids. The negative impacts on the fitness and performance of the subsequent aphids may have significant implications in virus transmission, distribution, and epidemiology.