Zn(II)(2)Cys(6) transcription factors are critical for the reproductive growth and sexual development of fungi, but their roles in Basidiomycota remain unclear. In this study, the Hypsizygus marmoreus gene hada-1 was shown to encode a Zn(II)(2)Cys(6) transcription factor, the growth rate of mycelia was decreased, hyphae were angulated, and fruiting body development was hindered in the hada-1-silenced strains. In addition, mitochondrial stability was lost, and the mitochondria morphologies changed from oval shaped to dumbbell or linear shaped in the silenced strains. Regarding mitochondrial instability, the mitochondrial complex II, III, and V activities and adenosine triphosphate content were significantly decreased. At the same time, the activities of the carbohydrate metabolism-related enzymes glucose-6-plosphatase, glucose dehydrogenase, and laccase were significantly decreased, which might have resulted in the reduction of carbon metabolism. Furthermore, hada-1 was shown to regulate the reactive oxygen species (ROS) level; compared with the wild-type (WT) strain, the silenced mycelia exhibited higher ROS contents and were more sensitive to oxidative stress. Taken together, these results indicate that, as a global regulator, hada-1 plays crucial roles in mycelial growth, fruiting body development, carbon metabolism, mitochondrial stability, and oxidative stress in the basidiomycete H. marmoreus.