Arbuscular mycorrhizal (AM) fungi facilitate plant uptake of mineral nutrients and draw organic nutrients from the plant. Organic nutrients are thought to be supplied primarily in the form of sugars. Here we show that the AM fungus Rhizophagus irregularis is a fatty acid auxotroph and that fatty acids synthesized in the host plants are transferred to the fungus to sustain mycorrhizal colonization. The transfer is dependent on RAM2 (REQUIRED FOR ARBUSCULAR MYCORRHIZATION 2) and the ATP binding cassette transporter–mediated plant lipid export pathway. We further show that plant fatty acids can be transferred to the pathogenic fungus Golovinomyces cichoracerum and are required for colonization by pathogens. We suggest that the mutualistic mycorrhizal and pathogenic fungi similarly recruit the fatty acid biosynthesis program to facilitate host invasion.