Blue light is a critical signal that triggers fruiting body initiation in mushroom-forming fungi. Pleurotus ostreatus is a cultivated model mushroom. The molecular mechanisms linking light perception to primordia formation remain poorly understood. We functionally characterized the blue light receptor gene PoWC-1, a homolog of Neurospora crassa white collar 1, during morphogenesis. Antisense-mediated silencing of PoWC-1 caused a delay in primordia formation under light/dark cycles and complete arrest at the undifferentiated mycelial stage under continuous darkness, underscoring its role in developmental progression. In darkness, PoWC-1 silencing downregulated key developmental transcription factors, hom1, hom2, Pofst3, and fst4, suggesting that PoWC-1 may contribute to developmental competence independently of light. Comparative transcriptomics revealed PoWC-1 influences a range of metabolic pathways—such as glycolysis/gluconeogenesis, the pentose phosphate pathway, and amino sugar metabolism—that may support the energetic and biosynthetic demands of fruiting initiation. In addition, PoWC-1 appears to affect upstream signaling components, including the MAPK pathway and the two-component system, along with a suite of downstream transcription factors. These findings suggest that PoWC-1 functions as a key regulator integrating blue light signals into a multi-layered network involved in metabolic reprogramming, signal transduction, and transcriptional regulation during primordia formation in P. ostreatus. Collectively, this study provides a molecular framework for understanding photomorphogenesis in edible mushrooms.