Light is a fundamental environmental factor for living organisms on earth—not only as a primary energy source but also as an informational signal. In fungi, light can be used as an indicator for both time and space to control important physiological and morphological responses. Botrytis cinerea (B. cinerea) is a devastating phytopathogenic fungus that exploits light cues to optimize virulence and the balance between conidiation and sclerotia development, thereby improving its dispersal and survival in ecosystems. However, the components and mechanisms underlying these processes remain obscure. Here, we identify a novel light-signaling component in B. cinerea, BcCfaS, which encodes a putative cyclopropane fatty-acyl-phospholipid synthase. BcCfaS is strongly induced by light at the transcriptional level and plays a crucial role in regulating photomorphogenesis. Deletion of BcCfaS results in reduced vegetative growth, altered colony morphology, impaired sclerotial development, and enhanced conidiation in a light-dependent manner. Moreover, the mutant exhibits serious defects in stress response and virulence on the host. Based on a lipidomics analysis, a number of previously unknown fungal lipids and many BcCfaS-regulated lipids are identified in B. cinerea, including several novel phospholipids and fatty acids. Importantly, we find that BcCfaS controls conidiation and sclerotial development by positively regulating methyl jasmonate (MeJA) synthesis to activate the transcription of light-signaling components, revealing for the first time the metabolic base of photomorphogenesis in fungi. Thus, we propose that BcCfaS serves as an integration node for light and lipid metabolism, thereby providing a regulatory mechanism by which fungi adapt their development to a changing light environment. These new findings provide an important target for antifungal design to prevent and control fungal disease.