<p>The ribosome biases the conformations sampled by nascent polypeptide chains along folding pathways toward biologically active states. A hallmark of the cotranslational folding (coTF) of many proteins constitutes highly stable folding intermediates that are absent or only transiently populated off the ribosome, yet persist during translation well beyond complete emergence of the domain from the ribosome exit tunnel. Despite the importance of intermediates for folding fidelity, their structures have remained elusive and cannot be predicted by machine learning methods. Here we obtained structures of two folding intermediates of an immunoglobulin-like domain on the ribosome by developing comprehensive ¹⁹F nuclear magnetic resonance analyses using chemical shifts by rational design, paramagnetic relaxation enhancement and protein engineering, integrated with extensive molecular dynamics simulations. The resulting intermediate structures reveal native-like folded cores distinguished by nonnative termini, permitting distinct binding to a molecular chaperone and suggesting parallel folding pathways. The structures of these intermediates are conserved within the protein domain family, in contrast to their in vitro refolding mechanisms. Our detailed structural ensembles of partially folded nascent proteins on the ribosome highlight the diversity of conformations sampled during coTF, providing the ribosome with a passive means to promote efficient protein folding and maintain cellular proteostasis.</p>