Genetically encoded voltage indicators (GEVIs) are a promising technology for visualizing the millisecond-scale dynamics of specific neuron types and their fine arbors in live animals, which presently neither electrophysiological nor Ca2+ imaging techniques do well. For researchers studying Drosophila, optical voltage imaging with GEVIs offers newfound possibilities to investigate cellular and sub-cellular electrophysiological phenomena that remain largely unexplored due to the technical difficulty of in vivo intracellular electrical recording methods. Here, to showcase the capabilities for optical voltage imaging in the intact fly brain, we imaged neuronal voltage dynamics in several parts of the fly olfactory system using our recently developed GEVI, Ace2N-mNeonGreen (Gong et al., Science 2015), in which a fast voltage-sensing domain from a rhodopsin family protein is coupled to a bright protein fluorophore through resonance energy transfer. Ace2N-mNeonGreen is sufficiently bright and fast to report neural action potentials and membrane voltage dynamics in awake flies, and resolves fast spike trains with 0.2-millisecond timing precision at spike detection error rates orders of magnitude better than prior GEVIs. In vivo imaging revealed sensory-evoked responses, including somatic spiking, dendritic dynamics, intracellular voltage propagation, and inter-hemispheric differences in neuronal activity. These results empower in vivo optical studies of neuronal electrophysiology and motivate novel experimental designs that will allow researchers to relate high-speed neuronal dynamics and information processing to fruit fly behavior..