Apicomplexan parasites such as Toxoplasma gondii depend on finely tuned cytoskeletal dynamics to invade and exit host cells. A central structure in this process is the conoid, a dynamic apical microtubule-based scaffold that integrates signalling and structural cues to initiate motility. While the lysine methyltransferase AKMT has been implicated in promoting the apical recruitment of the glideosome-associated connector (GAC), which links F-actin to surface adhesins, the broader methylation logic governing motility onset remains unclear. Here, we describe PCKMT, a second apically localized methyltransferase residing at the preconoidal rings, as essential for motility initiation. PCKMT enables the stable recruitment of the formin FRM1, whose actin-nucleating activity drives conoid extrusion and F-actin engagement with other components of the glideosome. In its absence, FRM1 fails to localise apically, conoid protrusion is impaired, and parasites are unable to glide, invade, or egress—despite normal replication and preserved conoid ultrastructure. In contrast, AKMT remains apically localised in PCKMT-deficient parasites but fails to relocalise upon motility activation—a process shown here to depend on FRM1 and actin dynamics. Although AKMT methylates numerous apical proteins, including cytoskeletal factors, the functional consequences of these modifications remain to be elucidated. Together, our findings define a dual methylation checkpoint at the parasite apex: PCKMT anchors FRM1 to license actin assembly, while AKMT reshapes apical architecture through actin-dependent disengagement and GAC recruitment. This layered regulatory system ensures that motility is initiated only when key components are in place, revealing an unappreciated role for lysine methylation in dynamic cellular remodelling.