The realization that transient population of partially unfolded conformations precedes the toxic aggregation of several amyloidogenic proteins has raised major interest in the design of compounds that could prevent protein misfolding. Long-range tertiary contacts offer a unique opportunity for the implementation of structure-based drug discovery strategies to find inhibitors of pathological protein aggregation. Representation of such transient contacts has, however, traditionally invoked the generation of low resolution and highly heterogeneous ensembles of structures that are impractical for in silico use. Here we show that it is possible to determine a single structural fold that describes at high resolution all tertiary contacts transiently established by the intrinsically disordered protein (IDP) α-synuclein under low and high amyloidogenic conditions. To generate the models we use paramagnetic relaxation enhancement (PRE) data as it directly probes transiently formed tertiary contacts, while being insensitive to other ensemble descriptors, such as size distribution, which are of little interest in docking studies. In our calculation strategy we refuse to comprehensively describe the conformational ensemble of the IDP (i.e. fulfilling average size and size distributions) in favor of maximizing the resolution in the description of the contacts interface. This high resolution structural representation shows that long-range contacts in α-synuclein result from interactions of residues with high average area buried upon folding and prominent tendency to aggregate in β-sheet structure. Our structural representation strategy condenses the tertiary contacts in a single fold, and as such, it has the potential to considerably accelerate rational drug discovery with amyloidogenic proteins and other disease-related IDPs.