This study integrates metagenomic and metabolomic data to systematically analyze the microbial community succession and carbon source metabolism transitions during the third fermentation cycle of Agaricus bisporus, with the aim of optimizing fermentation efficiency and lignocellulose degradation strategies. Principal Coordinate Analysis (PcoA) based on Bray–Curtis dissimilarity reveals significant microbial community separation across the stages of the first mushroom fruiting cycle. The overall pattern of “stage-specific differentiation” is consistent with the “cellulose hydrolysis” turn to the degradation of complex polysaccharides via carbohydrate-active enzymes (CAZymes). In the microbial network analysis showed that different microbe group controlled the stage-specific differentiation. These findings highlight a phase-dependent metabolic shift during the fermentation process: the early stages of fruiting rely more on cellulose-degrading microbes and their enzymatic systems, while later stages are driven by the degradation of complex polysaccharides and lignin derivatives, with Planctomycetota leading the degradation. This provides new mechanistic insights into agricultural waste resource utilization and the directional regulation of fermentation processes.