Kīlauea Volcano is an archetype for the complex interactions that can occur between a volcano’s summit and flanks. Decades of monitoring at Kīlauea have demonstrated that magma rises beneath the summit and flows laterally at shallow depths to erupt along the rift zones. Kīlauea’s recent eruptions at Halema‘uma‘u and Pu‘u ‘Ō‘ō mark the first time in the historic record that long-term (>1 year) eruptions have been concurrent at the summit and a rift zone, offering a new opportunity to improve our understanding of the relationship between these two segments of the magmatic system. While magma supply rate beneath the summit has been shown in previous studies to be a primary control on magmatic system pressure and eruptive activity, the role of the eruptive vent has been less clear. Our study shows that a dynamic equilibrium is maintained between Kīlauea’s summit and East Rift Zone (ERZ) eruptive vent—and lava lake level fluctuations are closely coupled at the two eruption sites—providing new constraints on the hydraulic connection and ERZ conduit. We show that localized changes at the ERZ eruption site during 2010-2011 regulated summit behavior in an uprift direction over distances of ~20 km. Changes in the elevation and efficiency of the ERZ vent affect pressure in Kīlauea’s magmatic system and impact summit behavior. Thus, the hydraulic connection between the summit and rift zone is a “two-way street” that transmits both downrift- and uprift-directed changes. Our results support recent work at other volcanoes that shows a complex interplay between a volcano’s summit reservoir and flank conduit during flank eruptions, and suggest that explosive summit activity may in some cases be triggered by changes far away on a volcano’s rift.