We present first solid insights on the origin, evolution and dispersal of citrus and elucidate the genealogy of the most important wild and cultivated varieties. These findings draw a new evolutionary framework for these fruit crops, a scenario that challenges current taxonomic and phylogenetic thoughts and points towards a reformulation of the genus Citrus. Based on genomic, phylogenetic and biogeographical analyses of the genus Citrus we propose that the center of origin of citrus was the Southeast foothills of the Himalayas, in a region including the eastern area of Assam, northern Myanmar and western Yunnan. Our analyses suggest that the ancestral citrus species underwent a sudden speciation during late Miocene and that the new species dispersed from there to surrounding regions, coinciding with a drastic transition from wetter monsoonal conditions to a drier climate. The Australian citrus and Tachibana mandarin split later from mainland citrus during the early Pliocene and Pleistocene, respectively.