After entry into the host cell, the intracellular parasite Toxoplasma gondii resides within a membrane-bound compartment, the parasitophorous vacuole (PV). The PV defines an intracellular, parasite-specific niche surrounded by host organelles, including the Golgi apparatus. The mechanism by which T. gondii hijacks the host Golgi and subverts its functions remains unknown. Here, we present evidence that the dense granule protein TgGRA3 interacts with host Golgi, leading to the formation of tubules and the entry of host Golgi material into the PV. Targeted disruption of the TgGRA3 gene delays this engulfment of host Golgi. We also demonstrate that TgGRA3 oligomerizes and binds directly to host Golgi membranes. In addition, we show that TgGRA3 dysregulates anterograde transport in the host cell, thereby revealing one of the mechanisms employed by T. gondii to recruit host organelles and divert their functions. This article has an associated First Person interview with the first author of the paper.