To explore the physical mechanisms that can guide spatial organization at biological membranes, we have constructed simple, cell-free intermembrane junctions. We find that the mechanically driven patterning of proteins uncovered in our earlier work can electrostatically generate spatial patterns in the distribution of charged membrane lipids. Tuning the magnitude of the interaction as a function of composition and ionic strength, and analyzing the interplay between thermodynamics and electrostatics via a Poisson-Boltzmann approach, we are able to determine the charge density and surface potential of the junction components. Surprisingly, the electrostatic potential of the proteins is a minor factor in the lipid reorganization; the protein size and its modulation of the junction topography play the dominant role in driving the electrostatic patterns.