Electrostatic fields generated on and inside biological membranes are recognized to play a fundamental role in key processes of cell functioning. Their understanding requires an adequate description on the level of elementary charges and the reconstruction of electrostatic potentials by integration over all elementary interactions. Out of all the available research tools, only molecular dynamics simulations are capable of this, extending from the atomic to the mesoscopic level of description on the required time and space scale. A complementary approach is that offered by molecular probe methods, with the application of electrochromic dyes. Highly sensitive to intermolecular interactions, they generate integrated signals arising from electric fields produced by elementary charges at the sites of their location. This review is an attempt to provide a critical analysis of these two approaches and their present and potential applications. The results obtained by both methods are consistent in that they both show an extremely complex profile of the electric field in the membrane. The nanoscopic view, with two-dimensional averaging over the bilayer plane and formal separation of the electrostatic potential into surface (Psi(s)), dipole (Psi(d)) and transmembrane (Psi(t)) potentials, is constructive in the analysis of different functional properties of membranes.