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Aims: Some biogeographical regions act primarily as donors of colonists to other regions, while others act predominantly as recipient areas. How some biotas become dominant while others do not is a largely historical question that has received surprisingly little attention from biogeographers. Here, we seek to answer this question for the cold‐water North Pacific biota, which did not exist forty million years ago but which is now the principal donor biota outside the tropics. Location: We focus on the cool‐temperate coastal North Pacific Ocean over the last 36.5 million years. Taxon: We consider all multicellular taxa for which adequate fossil, phylogenetic and biogeographical data exist. Methods: After placing North Pacific geographical events in the broader context of ocean gateways opening and closing elsewhere in the world, we discuss the history and factors affecting the planktonic and benthic productivity in the North Pacific based on a review and critical evaluation of the literature. A synthesis of primary sources was used to evaluate the origins and fates of North Pacific lineages, with special emphasis on movements to, within and from the North Pacific during the Cenozoic era. Results: During the Late Eocene to earliest Miocene, the cooling North Pacific received colonists from adjacent warm‐water regions and the cold Southern Hemisphere, where temperate conditions had existed since at least the Cretaceous. From the Miocene onward, the North Pacific biota began to spread to the Southern Hemisphere and through Bering Strait to the Arctic and North Atlantic Oceans. Within the North Pacific, lineages during the early cooling phases spread predominantly from west to east, but in the Early Middle Miocene this pattern reversed, with later expansions going in both directions. An increase in productivity, powered by the evolution of highly productive seaweeds and by consumers with high metabolic rates, accompanied the transformation of the North Pacific from a recipient to donor biota. Main conclusions: The North Pacific replaced the Southern Hemisphere temperate biota as the principal donor biota during the Miocene through a combination of increasing productivity, low magnitudes of extinction and intense competition and predation in an ocean basin with a long coastline. [ABSTRACT FROM AUTHOR]