The identification of epitopes involved in protein-protein interactions is essential for understanding protein structure and function. Large scale efforts – while identifying the interactions – did not always yield these epitopes, could not confirm most of the known interactions, and seemed particularly unsuccessful for native intrinsic membrane proteins. We have developed a fluidics-based approach (non steady-state kinetics) to obtain the broadest set of the epitopes interacting with a given target and applied it to a phage display methodology optimized for membrane proteins. Phages expressing a liver cDNA library were screened against a membrane protein (VDAC) reconstituted into liposomes and captured on a chip surface. The controlled fluidics was obtained by a SPR device (Surface Plasmon Resonance) that combined the advantages of working with minute reaction volumes and non equilibrium conditions. We demonstrate selective enrichment of binders and could even select for different binding affinities by fractionation of the selected outputs at various elution times. With VDAC as bait – a mitochondrial channel critical for cellular metabolism and apoptosis - we could find at least 40 % of its already reported ligands and independently confirmed 55 novel functional interactions, some of which fully blocked the channel. This highly efficient approach is generally applicable for any protein, and could be automated and up-scaled – even without the use of a SPR device. The epitopes directly identified by this method are useful not only for unraveling interactomes but also for drug design and therapeutics.