In the crowded environment of cells, proteins frequently encounter other proteins in many possible orientations. Most of these encounters are short-lived because the physicochemical properties of the two binding patches do not match. However, even for protein pairs that bind tightly, it is not an easy task to find the correct binding site on the partner protein and align with it. So far not well understood is the source of interaction specificity that favors a small set of specific "native" interactions over the multitude of alternative orientations. We used molecular dynamics simulations to study nonspecific complexes formed by barnase and barstar, cytochrome c and cytochrome c peroxidase, and the complex of the N-terminal domain of enzyme I with the histidine-containing phosphocarrier. We found that spontaneously forming nonspecific encounters involve interaction interfaces smaller than those of the specific complexes and are attracted by shorter-range direct interactions between the proteins.