Faithful chromosome segregation relies on precise kinetochore-microtubule interactions and checkpoint surveillance, yet the molecular basis of these processes varies widely across eukaryotes and is only beginning to be defined in apicomplexan parasites. In the malaria parasite Plasmodium berghei , chromosome segregation is especially critical during transmission from host to mosquito: rapid mitoses generate male gametes, and meiosis in the zygote seeds the next round of infection. Here, we identify Aurora-related kinase 1 (ARK1) as a central regulator of chromosome segregation in both mitotic and meiotic contexts. ARK1 localises to spindle poles, spindles, and kinetochores, and its depletion results in short and multipolar spindles, kinetochore misalignment, and failed chromosome partitioning. ARK1 forms a minimal Chromosomal Passenger Complex (CPC) with INCENP-A during male gametogenesis, but associates with additional components, including INCENP-B, kinetochores, centromeric histones, and spindle assembly checkpoint proteins, during meiosis. This stage-specific modularity supports efficient male gamete formation while safeguarding faithful chromosome inheritance during zygote development, thereby ensuring parasite transmission to the mosquito. Together, our findings indicate that P. berghei deploys distinct CPC states across sexual development, revealing developmental plasticity in chromosome-segregation control and a potential vulnerability for blocking transmission.