The phylum Apicomplexa comprises a large group of eukaryotic organisms that have evolved an obligate parasitic lifestyle. Major representatives such as Plasmodium falciparum, Cryptosporidium parvum and Toxoplasma gondii—the causative agents of malaria, cryptosporidiosis and toxoplasmosis, respectively—underline the major veterinary and medical importance of this phylum. A hallmark of all apicomplexan parasites is the presence of an apical complex, composed of cytoskeletal elements and specialized secretory organelles essential for motility and host cell invasion. In T. gondii, the apical complex includes the conoid, a tubulin-based cone topped by preconoidal rings (PCRs), which contain proteins essential for parasite motility and surround two short intraconoidal microtubules (ICMTs). These structures are connected to the apical polar ring (APR), a circular proteinaceous platform from which 22 subpellicular microtubules (SPMTs) emerge, providing shape and rigidity to the parasite. Secretory organelles, micronemes and rhoptries, discharge their contents through the conoid. Micronemes release adhesins and perforins required for egress, gliding motility, attachment and invasion, while rhoptries deliver factors required for establishment of infection. The conoid is dynamic and can be observed in extruded (during invasion and motility) or retracted states in intracellular resting parasites, a process known as conoid extrusion. During my thesis, I characterized multiple conoid components involved in its extrusion mechanism and required for parasite motility. Central to this process are the PCRs, which act as a structural hub for invasion factors and assembly of the glideosome. This actomyosin-dependent motility is tightly regulated, likely by controlling the apico-basal flux of filamentous actin (F-actin) into the pellicular space. Using ultrastructure expansion microscopy (U-ExM) combined with collaborative cryo-electron tomography on genetically modified parasites, I identified several APR proteins (APR2–APR7) contributing to the multilayered APR architecture. Depletion of APR2 blocked conoid extrusion and caused cytosolic leakage of F-actin, revealing a key role for the APR in sealing the connection between cytosol and pellicular space to ensure efficient F-actin channeling during invasion. Additionally, I uncovered a second function of the APR mediated by RNG2: parasites depleted of RNG2 detached their conoid from the apical complex upon extrusion stimulation, demonstrating that the APR mechanically tethers the conoid during extrusion and retraction. The apical complex is also assembled early during endodyogeny, in which two daughter cells form within the mother parasite. T. gondii contains five tubulin-based structures: the conoid, ICMTs, SPMTs, centrioles and spindle microtubules. By combining U-ExM and reverse genetics, I showed that the γ-tubulin complex localizes to the nascent conoid during division, and that γ-tubulin depletion prevents formation of all five tubulin-based structures, highlighting a shared nucleation mechanism. Finally, I investigated lysine methylation mediated by lysine methyltransferases (KMTs), a key post-translational modification affecting apical complex components. The apical complex lysine methyltransferase (AKMT), localized to PCRs and the conoid, is essential for conoid extrusion and parasite motility during induced egress.