Ruminant livestock contribute to atmospheric methane (CH4) from enteric microbial fermentation of feed in the reticulo-rumen. Our research aimed to increase understanding of how digestive characteristics and rumen anatomy of the host animal contribute to variation in CH4 emissions between individual sheep. In total, 64 ewes were used in an incomplete block experiment with four experimental test periods (blocks). Ewes were chosen to represent the diversity of phenotypic variation in CH4 emissions: there were at least 10 offspring from each of four sires and a range of liveweights. Throughout the experiment, the ewes were fed equal parts of lucerne and oaten chaff, twice daily, at 1.5 times the maintenance requirements. Daily CH4 emission (g/day) increased significantly (P < 0.001) with an increasing dry-matter intake (DMI) and reticulo-rumen volume (P < 0.001). Lower methane yield (g CH4/kg DMI) was associated with shorter mean retention times of liquid (r = 0.59; P < 0.05) and particle (r = 0.63; P < 0.05) phases of the digesta in the rumen. Significant between sire variation was observed in CH4 emissions and in rumen volume (P = 0.02), the masses of liquids (P = 0.009) and particles (P < 0.03) in the rumen and the proportion of gas in the dorsal sac of the rumen (P = 0.008). The best predictors of variation in CH4 emissions due to the host were DMI, CO2 emissions, rumen volume, liveweight, mean retention time of particles in the rumen, dorsal papillae density and the proportion of liquid in the contents of the rumen compartments.