The efficiency of microbial fuel cells (MFCs) in industrial wastewater treatment is profoundly influenced by the microbial community, which can be disrupted by variable industrial operations. Although microbial guilds linked to MFC performance under specific conditions have been identified, comprehensive knowledge of the convergent community structure and pathways of adaptation is lacking. Here, we developed a microbe-microbe interaction genome-scale metabolic model (mmGEM) based on metabolic cross-feeding to study the adaptation of microbial communities in MFCs treating sulfide-containing wastewater from a canned-pineapple factory. The metabolic model encompassed three major microbial guilds: sulfate-reducing bacteria (SRB), methanogens (MET), and sulfide-oxidizing bacteria (SOB). Our findings revealed a shift from an SOB-dominant to MET-dominant community as organic loading rates (OLRs) increased, along with a decline in MFC performance. The mmGEM accurately predicted microbial relative abundance at low OLRs (L-OLRs) and adaptation to high OLRs (H-OLRs). The simulations revealed constraints on SOB growth under H-OLRs due to reduced sulfate-sulfide (S) cycling and acetate cross-feeding with SRB. More cross-fed metabolites from SRB were diverted to MET, facilitating their competitive dominance. Assessing cross-feeding dynamics under varying OLRs enabled the execution of practical scenario-based simulations to explore the potential impact of elevated acidity levels on SOB growth and MFC performance. This work highlights the role of metabolic cross-feeding in shaping microbial community structure in response to high OLRs. The insights gained will inform the development of effective strategies for implementing MFC technology in real-world industrial environments.