Modern neuroscience and the interest in biomimetic control design demand increasingly sophisticated experimental techniques that can be applied in freely moving animals under realistic behavioral conditions. To explore sensorimotor flight control mechanisms in free-flying fruit flies (Drosophila melanogaster), we equipped a wind tunnel with a Virtual Reality (VR) display system based on standard digital hardware and a 3D path tracking system. We demonstrate the experimental power of this approach by example of a 'one-parameter open loop' testing paradigm. It provided (1) a straightforward measure of transient responses in presence of open loop visual stimulation; (2) high data throughput and standardized measurement conditions from process automation; and (3) simplified data analysis due to well-defined testing conditions. Being based on standard hardware and software techniques, our methods provide an affordable, easy to replicate and general solution for a broad range of behavioral applications in freely moving animals. Particular relevance for advanced behavioral research tools originates from the need to perform detailed behavioral analyses in genetically modified organisms and animal models for disease research.