Rhoptries are club-shaped, regulated secretory organelles that cluster at the apical pole of apicomplexan parasites. Their discharge is essential for invasion and the establishment of an intracellular lifestyle. Little is known about rhoptry biogenesis and recycling during parasite division. In Toxoplasma gondii, positioning of rhoptries involves the armadillo repeats only protein (TgARO) and myosin F (TgMyoF). Here, we show that two TgARO partners, ARO interacting protein (TgAIP) and adenylate cyclase β (TgACβ) localize to a rhoptry subcompartment. In absence of TgAIP, TgACβ disappears from the rhoptries. By assessing the contribution of each TgARO armadillo (ARM) repeat, we provide evidence that TgARO is multifunctional, participating not only in positioning but also in clustering of rhoptries. Structural analyses show that TgARO resembles the myosin-binding domain of the myosin chaperone UNC-45. A conserved patch of aromatic and acidic residues denotes the putative TgMyoF-binding site, and the overall arrangement of the ARM repeats explains the dramatic consequences of deleting each of them. Lastly, Plasmodium falciparum ARO functionally complements TgARO depletion and interacts with the same partners, highlighting the conservation of rhoptry biogenesis in Apicomplexa.