Owing to its great market potential for food and health care, whiteAuricularia cornea, a rare edible fungus, has received increased attention in recent years. This study presents a high-quality genome assembly ofA. corneaand multi-omics analysis of its pigment synthesis pathway. Continuous Long Reads libraries, combined with Hi-C-assisted assembly were used to assemble of whiteA. cornea. Based on this data, we analyzed the transcriptome and metabolome of purple and white strains during the mycelium, primordium, and fruiting body stages. Finally, we obtained the genome ofA.corneaassembled from 13 clusters. Comparative and evolutionary analysis suggests thatA.corneais more closely related toAuricularia subglabrathan toAuricularia heimuer. The divergence of white/purpleA.corneaoccurred approximately 40,000 years ago, and there were numerous inversions and translocations between homologous regions of the two genomes. Purple strain synthesized pigment via the shikimate pathway. The pigment in the fruiting body ofA. corneawas γ-glutaminyl-3,4-dihydroxy-benzoate. During pigment synthesis, α-D-glucose-1P, citrate, 2-Oxoglutarate, and glutamate were four important intermediate metabolites, whereas polyphenol oxidase and other 20 enzyme genes were the key enzymes. This study sheds light on the genetic blueprint and evolutionary history of the whiteA.corneagenome, revealing the mechanism of pigment synthesis inA.cornea. It has important theoretical and practical implications for understanding the evolution of basidiomycetes, molecular breeding of whiteA.cornea, and deciphering the genetic regulations of edible fungi. Additionally, it provides valuable insights for the study of phenotypic traits in other edible fungi.