The tachyzoite stage of the apicomplexan parasite Toxoplasma gondii divides by an internal budding process called endodyogeny. Single copy organelles like the apicoplast, Golgi, and the mitochondrion require a precise machinery to ensure that each daughter cell receives exactly one organelle. The T. gondii apicoplast is partitioned between the two daughters by temporal association with the centrosomes, which is the major hub orchestrating the various cell division processes. However, the identity of the molecular infrastructure facilitating anchoring of the apicoplast to the centrosome is still unknown. In this study, we describe the apicoplast partitioning protein 1 (APP1), a hypothetical protein that first assembles in a specific basal complex (BC) section and then localizes to a region in close proximity to the apicoplast. Conditional APP1 knockdown resulted in a specific apicoplast partitioning defect. Reciprocally, upon apicoplast loss through ATG8-depletion, APP1 remains localized to the cytoskeleton, consolidating a role in apicoplast anchoring to the cell division infrastructure. Using APP1 as bait in a proximity biotinylation screen, we identified several known proteins of the inner membrane complex (IMC) and the BC, highlighting its close association with the parasite’s unique cytoskeleton. We further characterized proteins of unknown function and identified APP3, which positions APP1 to the specific site on the BC, but has overall a more pleiotropic role in coordinating cell division. In summary, APPs are functional connectors between the apicoplast and the daughter cytoskeleton scaffold (DCS) critical for apicoplast inheritance. Together our findings provide novel mechanistic insights into this unique aspect of apicomplexan organelle biology.