Toxoplasma gondii, a widely prevalent human and animal pathogen and a relative of the malaria-causing Plasmodium spp., is a member of the phylum Apicomplexa encompassing a large number of single-celled eukaryotic organisms that are obligate endoparasites of animals. Apicomplexans evolved multiple adaptations to parasitism. One such distinctive feature of the apicomplexan cell, which the phylum is named after, is the apical complex comprising a battery of secretory vesicles and unusual cytoskeletal structures. The latter include the conoid, apical polar rings, and sub-pellicular microtubules. Functions of the apical cytoskeletal structures are poorly understood due to incomplete knowledge of their molecular composition. Furthermore, the conoid is believed to be heavily reduced or missing from Plasmodium species and other members of the class Aconoidasida. We have applied a spatial proteomic method called proximity-dependent biotin identification, BioID, to identify conoid-associated proteins in the model apicomplexan Toxoplasma gondii. We chose three proteins located at the apex of the T. gondii cell as BioID baits fused with the promiscuous biotin-ligase BirA*: SAS6L at the conoid, RNG2 linking the conoid and one of the apical polar rings, and MORN3 distributed at the apical subdomain of the inner membrane complex but excluded from the vicinity of the conoid. The enrichment of biotinylated proteins on streptavidin matrix in the BioID-bait cells relative to the untransformed parental cell line control was determined using a shotgun proteomic approach with label-free quantitation. The location of conoid protein candidates prioritised by BioID has been further validated by fluorescence microscopy in T. gondii tachyzoites and several life-cycle stages of P. berghei. Collectively we show that the conoid is a conserved apicomplexan element at the heart of the invasion mechanisms of these highly successful and often devastating parasites.