In Toxoplasma gondii , the conoid comprises a cone with spiraling tubulin fibers, preconoidal rings, and intraconoidal microtubules. This dynamic organelle undergoes extension and retraction through the apical polar ring (APR) during egress, gliding, and invasion. The forces involved in conoid extrusion are beginning to be understood, and its role in directing F-actin flux to the pellicular space, thereby controlling parasite motility, has been proposed. However, the contribution of the APR and its interactions with the conoid remain unclear. To gain insight into the APR architecture, ultrastructure expansion microscopy was applied to pinpoint known and newly identified APR proteins (APR2 to APR7). Our results revealed that the APR is constructed as a fixed multilayered structure. Notably, conditional depletion of APR2 resulted in significant impairments in motility and invasion. Electron microscopy and cryoelectron tomography revealed that depletion of APR2 alters APR integrity, affecting conoid extrusion and causing cytosolic leakage of F-actin. These findings implicate the APR structure in directing the apico-basal flux of F-actin to regulate parasite motility and invasion.