In eukaryotes, intracellular cargo transport typically involves molecular motors associating with the surface of membrane-bound cargo and transporting it along microtubule and actin tracks. In Toxoplasma gondii (T. gondii), intracellular cargo transport relies on actin and the unconventional myosin, myosin F (MyoF). Loss of MyoF disrupts vesicle transport, endomembrane organelle positioning, and apicoplast inheritance, yet the mechanism by which this actomyosin system's facilitates this process remains unclear. Using live-cell imaging, we determined that MyoF-EmFP has a dynamic and filamentous-like localization in the parasite cytosol, reminiscent of cytosolic actin filament dynamics. MyoF was not associated with Golgi, apicoplast or dense granule surfaces, suggesting that MyoF does not function using the canonical cargo transport mechanism. Instead, we find that loss of MyoF results in a dramatic rearrangement of the actin cytoskeleton in interphase parasites accompanied by significantly reduced actin dynamics, while actin organization during replication and motility were unaffected. Thus, these findings reveal that MyoF is an actin-organizing protein in T. gondii which facilitates cargo movement using an unconventional transport mechanism.