, commonly known as the mini oyster mushroom, is highly esteemed for its crisp texture and umami flavor. Limited genetic diversity among cultivars raises concerns regarding its sustainable industrial production. To delve into the maternal genetic diversity of the principal cultivars, 36 cultivars and five wild isolates were subjected to sequencing and assembly to generate high-quality mitogenome sequences. The mitogenomes had lengths ranging from 69,096 to 72,905 base pairs. The mitogenome sizes of and those of other mushroom species in genus showed a significant positive correlation with the counts of LAGLIDAG and GIY-YIG homing endonucleases encoded by intronic open reading frames. A comparison of gene arrangements revealed an inversion of a fragment containing between and . The mitogenomes of were clustered into three distinct clades, two of which were crowded with commercial cultivars. Clade I, all of which possess an inserted gene, shared a maternal origin linked to an ancestral cultivar from Taiwan. Primers were designed to target the gene, potentially safeguarding intellectual property rights. The wild isolates in Clade III exhibited more divergent mitogenomes, rendering them valuable for breeding.