Candida albicans can undergo heritable switching between two pathogenic cell types, white and opaque, which can persist across hundreds of generations. This transition is governed by the opaque master regulator Wor1, which initiates a highly intertwined transcriptional regulatory network resembling those that control cellular differentiation in higher eukaryotes. We find that Wor1 and additional white-opaque regulators are associated with the formation of opaque-specific super-enhancer-like elements that promote robust expression of target genes. These regulatory elements coincide with extensive chromatin remodeling, including eviction of “fragile” nucleosomes, which appears linked to the epigenetic “memory” of the opaque state. Notably, the white-to-opaque switch is correlated with large, macromolecular condensates of Wor1 in the nuclei of opaque cells, likely formed via liquid-liquid phase separation. Together, our findings suggest that Wor1-driven super-enhancers may assemble into transcriptional hubs that stabilize the opaque program, paralleling mechanisms that control lineage specification and cancer in higher eukaryotes.