Ligand discovery of nonenzymatic proteins can be accomplished through screening methods utilizing libraries comprising small molecules, peptides, and peptidomimetics. Incorporating peptoids, which are oligomers of -substituted glycine monomers, into high-throughput screens can produce libraries of large structural diversity. Due to their malleable structures, peptoids can occupy unique protein binding sites, but determination of the peptoid binding pose is challenging. For example, the peptoid KDT-11 is reported to bind with low micromolar binding affinity to the proteasome subunit Rpn-13. Poor solubility of initial compound screening hits, like KDT-11, can greatly hinder progress in drug discovery since it limits in vitro characterization. The work reported here overcomes this hurdle with the addition of a solubility tag to KDT11, enabling elucidation of the biologically relevant surface of the peptoid through a variety of structure-activity relationships and biophysical studies. NMR paramagnetic relaxation data guided a structural modeling protocol using multiple molecular dynamics (MD) trajectories and extensive sampling. The final peptoid-protein structure is conformationally stable in equilibrium MD trajectories for >1 μs time period. KDT-11 binds across the β6/β7/β8 strands and α-helix of Rpn-13, revealing an interface for inhibition that could be targeted in future computational drug discovery efforts to obtain more potent ligands for Rpn-13. It is reasonable that the methodology described here can extend to other flexible peptoid or peptide ligands in complexes with proteins.