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How the substantial climate shifts of the Cenozoic era shaped the geographical distribution of tropical cyclone genesis remains unknown. Through a set of coupled model simulations, we demonstrate that conditions during the warmer Early Eocene are more favorable for storm formation over the Southern Hemisphere, particularly the South Indian Ocean. As the climate cools, there is an increasing favorability for genesis in the Northern Hemisphere and a coincident decrease in the Southern Hemisphere over time, with the locations most conducive to storms migrating equatorward in both hemispheres. A shift in the most favorable conditions to the western North Pacific likely occurs during the Pliocene, largely due to the closure of the tropical seaways, and marks the final establishment of modern tropical cyclone distribution. The substantial variations of genesis regions in the Cenozoic may affect upper-ocean vertical mixing and hence tropical/global climate, but are missed in most current deep-time simulations.