Centrosomes are the main microtubule-organizing center of the cell. They are normally formed by two centrioles, embedded in a cloud of proteins known as pericentriolar material. The PCM ascribes centrioles with their microtubule nucleation capacity. Toxoplasma gondii, the causative agent of toxoplasmosis, divides by endodyogeny. Successful cell division is critical for pathogenesis. The centrosome, plays central roles in orchestrating the temporal and physical coordination of major organelle segregation and daughter cell formation. The T. gondii centrosome is formed by two domains; an outer core, distal from the nucleus, and an inner core, proximal to the nucleus. This dual organization has been proposed to underlie T. gondii’s cell division plasticity. However, the role of the inner core remains undeciphered. Here, we focus on the role of its only known molecular marker; TgCEP250L1. We show that upon conditional degradation of TgCEP250L1, parasites exhibit nuclear segregation defects, whilst normally forming daughter cells. In addition, the centrioles, disconnect from the nucleus. We explore the structural defects underlying these phenotypes by high resolution microscopy. We show that TgCEP250L1’s location is dynamic and encompasses the formation of the mitotic spindle. Moreover, we show that in the absence of TgCEP250L1, the microtubule binding protein TgEB1, fails to translocate from the nucleus to the mitotic spindle, while polyploid nuclei accumulate. Overall, our data supports a model in which the inner core of the T. gondii centrosome critically participates in cell division by directly impacting the formation or stability of the mitotic spindle.