Equine cumulus-oocyte complexes (COCs) are classified as compact (cCOC) or expanded (eCOC) and vary in their meiotic competence. This difference could be related to divergent glucose metabolism. To test this hypothesis in the present study, eCOCs, cCOCs and expanded or compact mural granulosa cells (EC and CC respectively) were matured in vitro for 30h, at which time maturation rate, glucose metabolism and the expression of genes involved in glucose transport, glycolysis, apoptosis and meiotic competence were determined. There were significant differences between eCOCs and cCOCs in maturation rate (50% vs 21.7% (n=192 and 46) respectively; P<0.001), as well as mean (±s.e.m.) glucose consumption (1.8±0.5 vs 27.9±5.9 nmol per COC respectively) and pyruvate (0.09±0.01 vs 2.4±0.8 nmol per COC respectively) and lactate (4.7±1.3 vs 64.1±20.6 nmol per COC respectively; P<0.05 for all) production. Glucose consumption in EC and CC did not differ significantly. Expression of hyaluronan-binding protein (tumour necrosis factor alpha induced protein 6; TNFAIP6) was increased in eCOCs and EC, and solute carrier family 2 member 1 (SLC2A1) expression was increased in eCOCs, but there were no differences in the expression of glycolysis-related enzymes and solute carrier family 2 member 3 (SLC2A3) between the COC or mural granulosa cell types. The findings of the present study demonstrate that metabolic and genomic differences exist between eCOCs and cCOCs and mural granulosa cells in the horse.