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Summary: During symmetry breaking, the highly conserved Rho GTPase Cdc42 becomes stabilized at a defined site via an amplification process. However, little is known about how a new polarity site is established in an already asymmetric cell—a critical process in a changing environment. The human fungal pathogen Candida albicans switches from budding to filamentous growth in response to external cues, a transition controlled by Cdc42. Here, we have used optogenetic manipulation of cell polarity to reset growth in asymmetric filamentous C. albicans cells. We show that increasing the level of active Cdc42 on the plasma membrane results in disruption of the exocyst subunit Sec3 localization and a striking de novo clustering of secretory vesicles. This new cluster of secretory vesicles is highly dynamic, moving by hops and jumps, until a new growth site is established. Our results reveal that secretory vesicle clustering can occur in the absence of directional growth. : Silva et al. use light-dependent plasma membrane recruitment of active Cdc42 to reset polarity in asymmetric filamentous fungal cells. This transient increase in plasma membrane active Cdc42 disrupted membrane traffic and resulted in the formation of a striking de novo secretory vesicle cluster, in the absence of directional growth. Keywords: polarity, optogenetics, Cdc42, membrane traffic, morphology, fungi