Membrane surface charge is critical for the transient, yet specific recruitment of proteins with polybasic regions to certain organelles. In eukaryotes, the plasma membrane (PM) is the most electronegative compartment of the cell, which specifies its identity. As such, membrane electrostatics is a central parameter in signaling, intracellular trafficking, and polarity. Here, we explore which are the lipids that control membrane electrostatics using plants as a model. We show that phosphatidylinositol-4-phosphate (PI4P), phosphatidic acidic (PA), and phosphatidylserine (PS) are separately required to generate the electrostatic signature of the plant PM. In addition, we reveal the existence of an electrostatic territory that is organized as a gradient along the endocytic pathway and is controlled by PS/PI4P combination. Altogether, we propose that combinatorial lipid composition of the cytosolic leaflet of organelles not only defines the electrostatic territory but also distinguishes different functional compartments within this territory by specifying their varying surface charges. •A charge gradient along the endocytic pathway defines an electrostatic territory•PA accumulates to a significant level at the PM, in a DAG kinase-dependent manner•The strong PM electrostatic field is powered by the additive effect of PI4P, PA, PS•Curvature and PS/PI4P-driven electrostatics act as a dual TGN targeting signal Platre et al. show that plant plasma membrane-derived compartments each have a distinct electrostatic signature, set up by a combinatorial code of anionic phospholipids. This “electrostatic code” may represent a fundamental patterning principle of the endomembrane system and be a key determinant in protein targeting.