Parasites of phylum Apicomplexa cause significant morbidity and mortality on a global scale. Central to the pathogenesis of these parasites is their ability to invade host cells through a junction formed by members of the apical membrane antigen (AMA) and rhoptry neck protein 2 (RON2) families localized to the parasite surface and host outer membrane, respectively. Here we structurally and functionally characterize Toxoplasma gondii AMA4 ( Tg AMA4), a highly divergent AMA protein. Structural analyses of Tg AMA4 in the apo and RON2 _L1 bound forms reveal a previously underappreciated level of molecular diversity at the parasite–host-cell interface that offers important insight into stage-dependent invasion strategies and yields a more comprehensive model of apicomplexan invasion.