Mitosis in eukaryotes involves reorganization of the nuclear envelope (NE) and microtubule-organizing centres (MTOCs). In Plasmodium , the causative agent of malaria, male gametogenesis mitosis is exceptionally rapid and divergent. Within 8 minutes, the haploid male gametocyte genome undergoes three replication cycles (1N to 8N), while maintaining an intact NE. Axonemes assemble in the cytoplasm and connect to a bipartite MTOC-containing nuclear pole and cytoplasmic basal body, producing eight flagellated gametes. The mechanisms coordinating NE remodelling, MTOC dynamics, and flagellum assembly remain poorly understood. Here, we identify the SUN1-ALLAN complex as a novel mediator of NE remodelling and bipartite MTOC coordination during Plasmodium male gametogenesis. SUN1, a conserved NE protein, localizes to dynamic loops and focal points near nuclear spindle poles. ALLAN, a divergent Allantoicase-like protein, has a location like that of SUN1 at nuclear MTOCs. SUN1 and ALLAN form a unique complex, detected by live-cell imaging, ultrastructural expansion microscopy, and interactomics. Deletion of either SUN1 or ALLAN gene disrupts nuclear MTOC organization, leading to basal body mis-segregation, defective spindle assembly, and impaired kinetochore attachment, but axoneme formation remains intact. Ultrastructural analysis revealed nuclear and cytoplasmic MTOC miscoordination, producing aberrant flagellated gametes lacking nuclear material. Sun1 deletion also alters parasite lipid composition, underscoring its role in NE homeostasis. These defects block parasite development in the mosquito and transmission, highlighting the essential functions of this complex. This study reveals a bipartite MTOC and a highly divergent mechanism of NE remodelling during Plasmodium male gametogenesis. The SUN1-ALLAN complex is an unusual adaptation of the LINC complex, in absence of canonical KASH-domain proteins in Plasmodium , providing new insights into the evolution of closed mitosis and highlighting potential targets for blocking malaria transmission.