Black band disease (BBD) is a cyanobacterial-dominated polymicrobial mat that propagates on and migrates across coral surfaces, necrotizing coral tissue. Culture-based laboratory studies have investigated cyanobacteria and heterotrophic bacteria isolated from BBD, but the metabolic potential of various BBD microbial community members and interactions between them remain poorly understood. Here we report genomic insights into the physiological and metabolic potential of the BBD-associated cyanobacterium Geitlerinema sp. BBD 1991 and six associated bacteria that were also present in the non-axenic culture. The essentially complete genome of Geitlerinema sp. BBD 1991 contains a sulfide quinone oxidoreductase gene for oxidation of sulfide, suggesting a mechanism for tolerating the sulfidic conditions of BBD mats. Although the operon for biosynthesis of the cyanotoxin microcystin was surprisingly absent, potential relics were identified. Genomic evidence for mixed-acid fermentation indicates a strategy for energy metabolism under the anaerobic conditions present in BBD during darkness. Fermentation products may supply carbon to BBD heterotrophic bacteria. Among the six associated bacteria in the culture, two are closely related to organisms found in culture-independent studies of diseased corals. Their metabolic pathways for carbon and sulfur cycling, energy metabolism, and mechanisms for resisting coral defenses suggest adaptations to the coral surface environment and biogeochemical roles within the BBD mat. Polysulfide reductases were identified in a Flammeovirgaceae genome (Bacteroidetes) and the sox pathway for sulfur oxidation was found in the genome of a Rhodospirillales bacterium (Alphaproteobacteria), revealing mechanisms for sulfur cycling, which influences virulence of BBD. Each genomic bin possessed a pathway for conserving energy from glycerol degradation, reflecting adaptations to the glycerol-rich coral environment. The presence of genes for detoxification of reactive oxygen species and resistance to antibiotics suggest mechanisms for combating coral defense strategies. This study builds upon previous research on BBD and provides new insights into BBD disease etiology.