Significance Plasmodium malaria parasites use a unique substrate-dependent locomotion, termed gliding motility, to migrate through tissues and invade cells. Previously, it was thought that the small labile invasive stages that invade erythrocytes, merozoites, use this motility solely to penetrate target erythrocytes. Here we reveal that merozoites use gliding motility for translocation across host cells prior to invasion. This forms an important preinvasion step that is powered by a conserved actomyosin motor and is regulated by a complex signaling pathway. This work broadens our understanding of the role of gliding motility and invasion in the blood and will have a significant impact on our understanding of blood stage host–pathogen interactions and parasite biology, with implications for interventions targeting erythrocyte invasion.