We investigated the muscle structure–function relationships that underlie the aerobic capacity of an insectivorous, small (~15 g) marsupial, Sminthopsis crassicaudata (Family: Dasyuridae), to obtain further insight into energy use patterns in marsupials relative to those in placentals, their sister clade within the Theria (advanced mammals). Disparate hopping marsupials (Suborder Macropodiformes), a kangaroo (Macropus rufus) and a rat-kangaroo (Bettongia penicillata), show aerobic capabilities as high as those of ‘athletic’ placentals. Equivalent muscle mitochondrial volumes and cardiovascular features support these capabilities. We examined S. crassicaudata to determine whether highly developed aerobic capabilities occur elsewhere in marsupials, rather than being restricted to the more recently evolved Macropodiformes. This was the case. Treadmill-trained S. crassicaudata attained a maximal aerobic metabolic rate ( or MMR) of 272 ml O2 min−1 kg−1 (N=8), similar to that reported for a small (~20 g), ‘athletic’ placental, Apodemus sylvaticus, 264 ml O2 min−1 kg−1. Hopping marsupials have comparable aerobic levels when body mass variation is considered. Sminthopsis crassicaudata has a basal metabolic rate (BMR) about 75% of placental values but it has a notably large factorial aerobic scope (fAS) of 13; elevated fAS also features in hopping marsupials. The of S. crassicaudata was supported by an elevated total muscle mitochondrial volume, which was largely achieved through high muscle mitochondrial volume densities, Vv(mt,f), the mean value being 14.0±1.33%. These data were considered in relation to energy use levels in mammals, particularly field metabolic rate (FMR). BMR is consistently lower in marsupials, but this is balanced by a high fAS, such that marsupial MMR matches that of placentals. However, FMR shows different mass relationships in the two clades, with the FMR of small (<125 g) marsupials, such as S. crassicaudata, being higher than that in comparably sized placentals, with the reverse applying for larger marsupials. The flexibility of energy output in marsupials provides explanations for this pattern. Overall, our data refute widely held notions of mechanistically closely linked relationships between body mass, BMR, FMR and MMR in mammals generally.