Genetically encoded fluorescent membrane potential probes constitute a critical prerequisite to image electrical activity from neuronal populations. The employment of previous genetically encoded probes has been restricted by their limited frequency response and/or low signal to noise ratio. Here we describe an alternative two-component hybrid probe consisting of a genetically encoded fluorescent protein (membrane anchored eGFP) combined with a synthetic voltage-sensing molecule (dipicrylamine, DPA). DPA is a small, non-fluorescent absorber that partitions into the membrane and distributes between the inner and outer leaflet according to the membrane potential due to its negative charge. The voltage-dependent translocation of the synthetic voltage sensor is translated via FRET into a large fluorescence signal (up to 34% change/100 mV) with a fast response and recovery time (0.5 ms). Using this two-component approach, we were able to optically record action potentials from neuronal cell lines and trains of action potentials from primary cultured neurons. Similar measurements carried out using fluorescently labeled antibodies suggest that these hybrid approaches may form the basis for a new generation of protein-based voltage probes.