SummaryRecent evidence shows that the arbuscular mycorrhizal (AM) symbiosis is established by two distinct groups of fungi, with the distinctive ‘fine root endophyte’ morphotype formed by fungi from the sub-phylum Mucoromycotina rather than the sub-phylum Glomeromycotina. While Mucoromycotina AM are abundant and globally distributed, there is currently no understanding of the genomic basis for the symbiosis or how this compares to other mycorrhizal symbionts.We used culture-independent metagenome sequencing to assemble and characterise the metagenome-assembled genome (MAG) of a putative fine root endophyte, which we show belonged to the family Planticonsortiaceae within the order Densosporales.The MAG shares key traits with Glomeromycotina fungi, which indicate obligate biotrophy, including absence of fatty acid and thiamine biosynthesis pathways, limited enzymatic abilities to degrade plant cell walls, and a high abundance of calcium transporters, chitin and mannan degrading genes. In contrast to Glomeromycotina fungi, it exhibited a higher capacity for degradation of microbial cell walls, a complete cellulose degradation pathway, low abundances of copper, nitrate and ammonium transporters, and a complete pathway for vitamin B6 biosynthesis.These differences highlight the potential for contrasting interactions between Mucoromycotina and Glomeromycotina AM fungi with their host plant and the environment which could support niche differentiation and complementary ecological functions.