The Plasmodium proteasome represents a potential antimalarial drug target for compounds with activity against multiple life cycle stages. We screened a library of human proteasome inhibitors (peptidyl boronic acids) and compared activities against purified P. falciparum and human 20S proteasome. We identified a series of potent parasite-active compounds that show a range of selectivity for inhibition of the growth of P. falciparum compared with human cell lines. To further validate the target, we selected P. falciparum for resistance in vitro to the clinically used boronate proteasome inhibitor, bortezomib. Whole genome sequencing revealed mutations in the proteasome b5 binding site. Two of the novel compounds that target both b2 and b5 of P. falciparum proteasome retain activity against the bortezomib resistant line, providing a key advantage for further development. A medicinal chemistry program is currently underway to improve the specificity of inhibitors based on the hits we identified. In addition, we have undertaken structural studies of the Plasmodium proteasome in complex with the PA28 activator. The structure of the P. falciparum PA28 regulator (PfPA28) was solved by X-ray crystallography. We purified Pf20S proteasome from parasite cultures and showed that PfPA28 readily forms single and double capped complexes with Pf20S. We structurally characterised the Pf20S-PfPA28 complex using cryo-EM. The structural information will help to provide a better understanding of the proteasomal system in P. falciparum and aid the design of more selective inhibitors.