Plasmodium falciparum is the causative agent of malaria and remains a pathogen of global importance. Asexual blood stage replication, via a process called schizogony, is an important target for the development of new antimalarials. Here we used Airyscan super resolution imaging coupled with ultrastructure-expansion microscopy to probe the organization and function of the chromosome-capturing kinetochores in relation to the mitotic spindle, the centriolar plaque and the apical organelles during schizont development. We provide evidence that the inner and outer domains of the centriolar plaque nucleate the spindle and cytoplasmic microtubules, respectively. This, in turn, provides a physical nexus between the mitotic apparatus and the apical complex. Conditional disruption of the kinetochore components, PfNDC80 and PfNuf2, causes aberrant mitotic spindle assembly and disrupted karyokinesis. Surprisingly, kinetochore disruption also leads to disengagement of the centrin-containing, outer centriolar plaque from the nuclear envelope. Severing the connection between the nucleus and the apical complex leads to the formation of merozoites lacking nuclei. The data suggest that correct assembly of the kinetochore/ spindle complex plays a previously unrecognised a role in positioning the nascent apical complex in developing P. falciparum merozoites.