Arbuscular mycorrhizal (AM) fungi - Glomeromycota and Endogonomycetes - comprise multiple species and higher-level taxa that have remained undescribed. We propose a mixed morphology- and DNA-based classification framework to promote taxonomic communication and shed light into the phylogenetic structure of these ecologically essential fungi. Based on eDNA samples and long reads as type materials, we describe 15 new species and corresponding genera (Pseudoentrophospora kesseensis, Hoforsa rebekkae, Kahvena rebeccae, Kelottijaervia shannonae, Kungsaengena shadiae, Langduoa dianae, Lehetua indrekii, Lokruma stenii, Moostea stephanieae, Nikkaluokta mahdiehiae, Parnigua craigii, Riederberga sylviae, Ruua coralieae, Tammsaarea vivikae and Unemaeea nathalieae), the genus Parvocarpum as well as 19 families (Pseudoentrophosporaceae, Hoforsaceae, Kahvenaceae, Kelottijaerviaceae, Kungsaengenaceae, Langduoaceae, Lehetuaceae, Lokrumaceae, Moosteaceae, Nikkaluoktaceae, Parniguaceae, Riederbergaceae, Ruuaceae, Tammsaareaceae, Unemaeeaceae, Bifigurataceae, Planticonsortiaceae, Jimgerdemanniaceae and Vinositunicaceae) and 17 orders (Hoforsales, Kahvenales, Kelottijaerviales, Kungsaengenales, Langduoales, Lehetuales, Lokrumales, Moosteales, Nikkaluoktales, Parniguales, Riederbergales, Ruuales, Tammsaareales, Unemaeeales, Bifiguratales and Densosporales), and propose six combinations (Diversispora bareae, Diversispora nevadensis, Fuscutata cerradensis, Fuscutata reticulata, Viscospora deserticola and Parvocarpum badium) based on phylogenetic evidence. We highlight further knowledge gaps in the phylogenetic structure of AM fungi and propose an alphanumeric coding system for preliminary communication and reference-based eDNA quality-filtering of the remaining undescribed genus- and family-level groups. Using AM fungi as examples, we hope to offer a sound, mixed framework for classification to boost research in the alpha taxonomy of fungi, especially the “dark matter fungi”.