The growth habit of mistletoes, the only woody, parasitic plants to infect host canopies, represents a key innovation. How this aerially parasitic habit originated is unknown; mistletoe macrofossils are relatively recent, from long after they adapted to canopy life and evolved showy, bird-pollinated flowers; sticky, bird-dispersed seeds; and woody haustoria diverting water and nutrients from host branches. Since the transition to aerial parasitism predates the origin of mistletoes’ contemporary avian seed dispersers by 20–40 million years, this leaves unanswered the question of who the original mistletoe dispersers were. By integrating fully resolved phylogenies of mistletoes and aligning the timing of historic events, I identify two ancient mammals as likely candidates for planting Viscaceae and Loranthaceae in the canopy. Just as modern mouse lemurs and galagos disperse viscaceous mistletoe externally (grooming the sticky seeds from their fur), Cretaceous primates (e.g., Purgatorius) may have transported seeds of root-parasitic understory shrubs up into the canopy of Laurasian forests. In the Eocene, ancestors of today’s mistletoe-dispersing marsupials, Dromiciops, likely fed on the nutritious fruit of root-parasitic loranthaceous shrubs, depositing the seeds atop western Gondwanan forest crowns. Once mistletoes colonized the canopy, subsequent evolution and diversification coincided with the rise of nectar-and fruit-dependent birds.