Fungus-farming (attine) ant agriculture is made up of five known agricultural systems characterized by remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Here we describe the first case of a lower-attine ant cultivating a higher-attine fungus based on our discovery of a Brazilian population of the relictual fungus-farming ant Apterostigma megacephala, known previously from four stray specimens from Peru and Colombia. We find that A. megacephala is the sole surviving representative of an ancient lineage that diverged similar to 39 million years ago, very early in the similar to 55-million-year evolution of fungus-farming ants. Contrary to all previously known patterns of ant-fungus symbiont fidelity, A. megacephala cultivates Leucoagaricus gongylophorus, a highly domesticated fungal cultivar that originated only 2-8 million years ago in the gardens of the highly derived and recently evolved (similar to 12 million years ago) leaf-cutting ants. Because no other lower fungus-farming ant is known to cultivate any of the higher-attine fungi, let alone the leaf-cutter fungus, A. megacephala may provide important clues about the biological mechanisms constraining the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture.National Science Foundation (NSF)National Museum of Natural History (NMNH)Smithsonian Institution Scholarly Studies ProgramCosmos Club FoundationFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Smithsonian Institution, Department of Entomology, National Museum of Natural HistoryUniversity of Maryland, Maryland Center for Systematic Entomology, Department of EntomologyUniversidade Federal de Uberlandia, Instituto de BiologiaUniversity of Texas at Austin, Department of Integrative BiologyUniversidade Estadual Paulista, Centro de Estudos de Insetos Sociais de Rio ClaroNSF: DEB-0949689NSF: DEB-0919519FAPESP: 2011/50226-0CNPq: 311562/2012-4CNPq: 487639/2012-0