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Mushroom-forming fungi in the order Agaricales represent an independent origin of bioluminescence in the tree of life, yet the diversity, evolutionary history, and timing of the origin of fungal luciferases remain elusive. We sequenced the genomes and transcriptomes of five bonnet mushroom species ( Mycena spp.), a diverse lineage comprising the majority of bioluminescent fungi. Two species with haploid genome assemblies ∼150Mb are amongst the largest in Agaricales, and we found that a variety of repeats between Mycena species were differentially mediated by DNA methylation. We show that bioluminescence evolved in the last common ancestor of mycenoid and the marasmioid clade of Agaricales and was maintained through at least 160 million years of evolution. Analyses of synteny across genomes of bioluminescent species resolved how the luciferase cluster was derived by duplication and translocation, frequently rearranged and lost in most Mycena species, but conserved in the Armillaria lineage. Luciferase cluster members were co-expressed across developmental stages, with highest expression in fruiting body caps and stipes, suggesting fruiting-related adaptive functions. Our results contribute to understanding a de novo origin of bioluminescence and the corresponding gene cluster in a diverse group of enigmatic fungal species. Significance We present the genomes of five new bonnet mushroom Mycena species, formerly the last fungal bioluminescent lineage lacking reference genomes. These genome-scale datasets allowed us to construct an evolutionary model pinpointing all possible changes in the luciferase cluster across all fungi and additional genes involved in bioluminescence. We show that luciferase clusters were differentially lost in different fungal lineages and in particular a substantial loss was observed in the Mycena lineage. This can be attributed to genome regions of Mycena underwent different evolutionary dynamics. Our findings offer insights into the evolution of how a gene cluster that emerged 160 million years ago and was frequently lost or maintained due to differences in genome plasticity. ### Competing Interest Statement The authors have declared no competing interest.

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