The polarized actin cable from the Spitzenkörper at the hyphal tip fuels filamentous growth in diverse biphasic fungal pathogens. This multicomponent complex, featuring the actin nucleator Bni1 and its associated actin regulator, initiates actin polymerization, guiding biphasic fungal growth and host infection. How dynamic assembly of the Spitzenkörper and actin cable is achieved to support filamentous fungi that undergo multistage morphogenesis for host invasion remains unclear. These fungi include Magnaporthe oryzae (M. oryzae), which undergoes a multistage morphological transition during host plant infection. Here, we showed that the M. oryzae scaffolder protein MoSpa2 remodels actin cable networks in space and time by assembling the polarisome complex via phase separation, thereby supporting polarized growth in M. oryzae. Via its N-terminal intrinsically disordered regions, MoSpa2 first stimulates actin cable assembly through multivalent interactions with the MoBni1 nucleator, after which it creates polarized actin cable bundles by association with F-actin and a concurrent inhibition of cofilin-mediated F-actin depolymerization. MoSPA2 mutants exhibit impaired hyphal growth and a reduced ability to infect host plants, underling the significance of this scaffolder. Overall, this work elucidates the fundamental mechanisms underlying fungal morphogenesis, offering the potential for targeted interventions in pathogenesis.