Plant viruses can change hosts in ways that increase vector contacts, virion acquisition, and subsequent vector dispersal to susceptible hosts. Based on this, researchers have proposed that virus-induced phenotypes are the product of adaptations to "manipulate" hosts in ways that increase transmission. Theoretical models of virus spread in crops support this proposition; "manipulative" viruses spread faster and to a greater extent. However, both empirical and theoretical studies on manipulation are disproportionately focused on a few persistently transmitted pathogens and rarely consider the broader ecological implications of virus infections. To address these knowledge gaps, we documented the effects of different stages of infection by an economically devastating, semi-persistently transmitted crinivirus, Cucurbit yellow stunting disorder virus [CYSDV] on Cucumis melo (muskmelon) phenotypes, behavior and performance of whitefly vectors (Bemisia tabaci) and non-vector aphid competitors (Aphis gossypii). Whiteflies were strongly attracted to CYSDV-infected hosts in a symptomatic stage of disease, but not in an asymptomatic stage, and fed more easily on infected plants regardless of symptoms. In contrast, aphids tended to avoid infected hosts, fed for shorter periods of time, and produced fewer offspring on infected hosts. Metabolomics revealed that host manipulations by CYSDV do not rely on virus-induced shifts in leaf primary metabolites or volatiles but may involve changes to phloem architecture and other compounds not measured here. Our study demonstrates a sophisticated host manipulation by CYSDV, whereby infection discourages colonization by a non-vector competitor while inducing a suite of progressively more transmission-conducive changes that encourage virion acquisition by the vector.