Twenty years since publication of the Plasmodium falciparum and P. berghei genomes one-third of their protein-coding genes lack functional annotation. In the absence of sequence and structural homology, protein-protein interactions can facilitate functional prediction of such orphan genes by mapping protein complexes in their natural cellular environment. The Plasmodium NPC (nuclear pore complex) is a case in point: it remains poorly defined; its constituents lack conservation with the 30+ proteins described in the NPC of many opisthokonts, a clade of eukaryotes that includes fungi and animals, but not Plasmodium. Here we developed a labeling methodology based on TurboID fusion proteins, which allows visualization of the berghei NPC and facilitates the identification of its components. Following affinity purification and mass spectrometry we identify four known Nups (138, 205, 221, and the bait 313) and verify interaction with the putative FG Nup637; we assign five proteins lacking annotation (and therefore meaningful homology with proteins outside the genus) to the NPC, which is confirmed by GFP tagging. Based on gene deletion attempts, all new Nups  Nup176, 269, 335, 390, and 434  are essential to parasite survival. They lack primary sequence homology with proteins outside the Plasmodium genus; albeit two incorporate short domains with structural homology to human Nup155 and yeast Nup157, and the condensin SMC4. The protocols developed here showcase the power of proximity-labeling for elucidating protein complex composition and annotation in Plasmodium. It opens the door to exploring the function of the Plasmodium NPC and understanding its evolutionary position.