Amanita muscaria sensu lato has a wide geographic distribution, occurring in Europe, Asia, Africa, Australia, New Zealand, and North, Central and South America. Previous phylogenetic work by others indicates three geographic clades (i.e. ‘Eurasian’, ‘Eurasian-alpine’ and ‘North American’ groups) within A. muscaria. However, the historical dispersal patterns of A. muscaria remained unclear. In our project, we collected specimens from arctic, boreal and humid temperate regions in Alaska, and generated DNA sequence data from the protein-coding beta-tubulin gene and the internal transcribed spacer (ITS) and large subunit (LSU) regions of the ribosomal DNA repeat. Homologous sequences from additional A. muscaria isolates were downloaded from GenBank. We conducted phylogenetic and nested clade analyses (NCA) to reveal the phylogeographic history of the species complex. Although phylogenetic analyses confirmed the existence of the three above-mentioned clades, representatives of all three groups were found to occur sympatrically in Alaska, suggesting that they represent cryptic phylogenetic species with partially overlapping geographic distributions rather than being allopatric populations. All phylogenetic species share at least two morphological varieties with other species, suggesting ancestral polymorphism in pileus and wart colour pre-dating their speciations. The ancestral population of A. muscaria likely evolved in the Siberian–Beringian region and underwent fragmentation as inferred from NCA and the coalescent analyses. The data suggest that these populations later evolved into species, expanded their range in North America and Eurasia. In addition to range expansions, populations of all three species remained in Beringia and adapted to the cooling climate.