Over the past two decades, grape production in North America has been threatened by the presence of red blotch, a viral disease impacting the production and profitability of vineyards. Grapevine red blotch virus (GRBV), the causative agent of the disease, is primarily disseminated via infected planting material. However, secondary spread has been observed in northern California and southern Oregon vineyards. Spissistilus festinus [Say, 1830] (Hemiptera: Membracidae), the three-cornered alfalfa hopper, is the only known vector of GRBV. It is also the first treehopper known to transmit a virus of grapevines, and the second treehopper species to transmit a plant virus. However, S. festinus is not a direct pest of grapevines and little is known in regard to the host-virus-vector interaction dynamics within the red blotch pathosystem. I first investigated attributes of GRBV transmission by S. festinus using time course experiments to track the movement of GRBV through the body of S. festinus. My results documented a circulative mode for transmission, with a 10-day acquisition access period (AAP) on wine grapes required for GRBV to be detectable in the salivary glands of S. festinus. Although S. festinus was known to acquire GRBV from infected, wine grape cultivars in greenhouse and vineyard settings, the role of GRBV-infected free-living Vitis species in disease epidemiology was not known. In vineyard ecosystems, free-living grapevines harbor GRBV in northern California suggesting that S. festinus can move GRBV to, from, and in-between free-living and cultivated vines. Thus, I conducted transmission assays using both cultivated and free-living vines and validated the movement of GRBV by S. festinus among the two Vitis species. Moreso, I analyzed the gut content of S. festinus specimens collected in northern California vineyards over two growing seasons and found V. californica DNA sequences in specimens carrying GRBV, demonstrating the ability of free-living vines to serve as a viral reservoir. In addition, I tracked the dietary history of S. festinus by analyzing the gut content of specimens caught in vineyard ecosystems and determined various feeding, reproductive, and overwintering hosts, informing the landscape-level movement of S. festinus in northern California vineyards. Lastly, S. festinus is a dimorphic insect with males and females behaving differently in their flight capacities and propensities. To better understand how distinct movement behaviors affect GRBV spread, I monitored dispersal patterns, as well as GRBV acquisition and transmission by males and females in arenas with detached snap bean trifoliates. Results revealed that S. festinus males are major contributors to spread of GRBV and that secondary spread is primarily related to walking and jumping dispersal behaviors of S. festinus. My findings provided new insights into the ecology and behavior of S. festinus in relation to GRBV transmission and red blotch disease epidemiology. These have been salient for providing growers with informed disease management recommendations focusing on the removal of inoculum sources, including free-living vines, rather than control of S. festinus populations.