The identification of ever-increasing numbers of RNA species has underlined the importance of robust characterization of bona fide sites of protein-RNA interaction. UV crosslinking can be used to identify precise RNA targets for individual proteins, transcriptome-wide. Here we sought to generate reciprocal data, identifying precise sites of RNA-binding proteome-wide. The resulting technique, identification of RNA-associated peptides (iRAP), was used to locate 1331 unique RNA-interaction sites at single amino acid residue resolution in 324 S. cerevisiae proteins. Our identified RNA-interaction sites in characterized RNA-protein complex agree well with available high-resolution structures. In known RNA-interacting protiens, 317 sites fall into known and suspected RNA-interaction domains while only 21 sites fall into other annotated sequence features. Strikingly, 993 of the sites identified fall into protein regions that lack any recognizable protein domain structure or annotated sequence features. This suggests that, despite binding RNA in vivo, many of these proteins will not have defined functions in RNA metabolism.