Methane is the end product of plant biomass anaerobic fermentation, however, on a per unit of feed basis, the quantity of this potent greenhouse gas produced varies between herbivorous animals. Foregut fermenters such as macropod marsupials (kangaroos, wallabies) represent a group of low methane emitting herbivores, compared to high methane producing ruminants. However, our understanding of the marsupial gut microbiome and the reasons for this low methane economy compared to ruminants is currently limited. Here, we present a metagenome-based analysis of the faecal community of 14 different marsupial hosts, focusing on the functional distinction of the bacterial and archaeal communities compared to ruminant hosts. Although the marsupial archaeal community composition from this dataset varied both between individual animals and species, archaea present with sufficient abundance for genome recovery and metabolic inference included hydrogenotrophic (e.g. Methanobrevibacter and Methanocorpusculum spp.) and/or methylotrophic methane producers (e.g. Methanosphaeara spp., Methanarcanum hacksteinii, UBA71 spp.). Using marker-gene-based community profiling, one archaeal species, the hydrogenotrophic Methanobrevibacter_A sp900769095 was positively associated with marsupials in comparison to ruminant faecal samples. In contrast, a clear host-associated signature for the bacterial community was found, which differs significantly between marsupial hosts and compared to ruminants. Gene-centric analysis of hydrogen metabolism pathways identified enrichment of key methanogenesis markers and methanogenesis-linked hydrogenases in ruminants. In contrast, hydrogen metabolism genes enriched in marsupials were bacterial in origin, including H2-uptake hydrogenases, enzymes involved in butyrate and propionate metabolism, along with nitrate and nitrite reductases, enzymes of ammonia assimilation and glutamate metabolism, all of which can support increased operation of alternate hydrogen sinks over methanogenesis. Overall, these data support a low-methane phenotype for marsupials involves enrichment of alternate hydrogen utilisation pathways of bacterial origin to methanogenesis, offering a genetic basis in pursuit of reduced methane emissions from rumen fermentation.