Grapevine red blotch is an emerging disease that threatens vineyard productions in North America. Grapevine red blotch virus (GRBV, species Grablovirus vitis, genus Grablovirus, family Geminiviridae), the causal agent of red blotch disease, is transmitted by Spissistilus festinus (Hemiptera: Membracidae) in a circulative, non-propagative mode. To gain new insight into GRBV-S. festinus interactions, we delved into vertical transmission and documented a lack of transovarial transmission. In addition, we investigated S. festinus sex differences in the horizontal transmission of GRBV by creating small arenas with 30 detached trifoliates of common snap bean, an experimental host of GRBV, and a preferred feeding host of S. festinus. Tracking the movement of viruliferous males, females, or a combination of the two sexes over two weeks in replicated experiments demonstrated that male S. festinus dispersed more than females with specimens of both sexes predominantly grouping together on trifoliates spatially surrounding the trifoliate onto which they were released. These behaviors resulted in a greater rate of GRBV transmission by S. festinus males (17%, 20 of 120) than females (4%, 5 of 120) or mixed-sex cohorts (9%, 17 of 180). In arenas with aviruliferous S. festinus and one (single) or four (hotspot) GRBV-infected trifoliates out of 30 total trifoliates, a higher GRBV transmission rate by males was confirmed in both single infection (50%, 30 of 60) and hotspot infection (83%, 50 of 60) arenas than by females in single infection (35%, 21 of 60) and hotspot infection (67%, 40 of 60) arenas. These findings highlighted sex-associated differences in the transmission of GRBV by S. festinus and a positive correlation between the initial virus prevalence and the rate of transmission. Finally, the secondary spread of GRBV resulted primarily from S. festinus dispersal by walking or jumping. Together, these unique GRBV transmission features support the need to characterize dispersal behaviors of S. festinus in vineyard ecosystems.