Summary Most contemporary angiosperms (flowering plants) are insect pollinated, but pollination by wind, water or vertebrates occurs in many lineages. Though evidence suggests insect pollination may be ancestral in angiosperms, this is yet to be assessed across the full phylogeny. Here, we reconstruct the ancestral pollination mode of angiosperms and quantify the timing and environmental associations of pollination shifts. We use a robust, dated phylogeny and species‐level sampling across all angiosperm families to model the evolution of pollination modes. Data on the pollination system or syndrome of 1160 species were collated from the primary literature. Angiosperms were ancestrally insect pollinated, and insects have pollinated angiosperms for c. 86% of angiosperm evolutionary history. Wind pollination evolved at least 42 times, with few reversals to animal pollination. Transitions between insect and vertebrate pollination were more frequent: vertebrate pollination evolved at least 39 times from an insect‐pollinated ancestor with at least 26 reversals. The probability of wind pollination increases with habitat openness (measured by Leaf Area Index) and distance from the equator. Our reconstruction gives a clear overview of pollination macroevolution across angiosperms, highlighting the long history of interactions between insect pollinators and angiosperms still vital to biodiversity today.

Pollination is a fundamental process driving the speciation of angiosperms (flowering plants). Most contemporary angiosperms are insect pollinated, but abiotic pollination by wind or water and vertebrate pollination by birds or mammals occurs in many lineages. We model the evolution of pollination across angiosperms and quantify the timing and environmental associations of pollination shifts. We use a robust dated phylogeny and trait-independent species-level sampling across all families of angiosperms to model the evolution of pollination modes. Data on the pollination system or syndrome of 1160 species were collated from primary literature. Angiosperms were ancestrally insect pollinated, and insects have pollinated angiosperms for approximately 86% of angiosperm evolutionary history. Wind pollination evolved at least 42 times, with few reversals back to animal pollination. Transitions between insect and vertebrate pollination were more frequent: vertebrate pollination evolved at least 39 times from an insect pollinated ancestor with at least 26 reversals. The probability of wind pollination increases with habitat openness (measured by Leaf Area Index) and with distance from the equator. Our reconstruction of pollination across angiosperms sheds light on a key question in angiosperm macroevolution, highlighting the long history of interactions between insect pollinators and angiosperms still vital to global biodiversity today.