Over 80 species are recognized in the commercially important genus Morchella, many of them endemic to specific regions or continents. Among them, M. anatolica and M. rufobrunnea are the earliest diverging lineages and are key in decoding the evolutionary history, global biogeography, and ecological trends within this iconic genus. Early ancestral area reconstruction (AAR) tests postulated a western North American origin of morels but had not included in the analyses M. anatolica, whose phylogenetic identity remained at the time unresolved. Following new collections of M. anatolica and M. rufobrunnea from the Mediterranean islands of Cyprus, Kefalonia, Lesvos, Malta, and Zakynthos, we performed revised AAR tests to update the historical biogeography of the genus. Our results, inferred from multilocus analysis of an expanded data set of 79 phylospecies, challenge previous reconstructions and designate the Mediterranean basin as the most likely place of origin for morels. Detailed morphoanatomical analyses demonstrate that ascocarp rufescence, the nondarkening apothecial ridges, the absence of a sinus, and the stipe pruinescence are all stable synapomorphic features of sect. Rufobrunnea, which could be interpreted as ancestral for the genus. The saprotrophic mode of nutrition, suggested by the prolific in vitro growth of M. anatolica, might also be an ancestral trait. Emended descriptions, including extensive imagery and scanning electron microscopy, are provided, and a new evolutionary hypothesis of the genus is proposed.