The harvest of plant parts and exudates from wild populations contributes to the income, food security and livelihoods of many millions of people worldwide. Frankincense, an aromatic resin sourced from natural populations of Boswellia trees and shrubs, has been cherished by world societies for centuries. Boswellia populations are threatened by over-exploitation and ecosystem degradation, jeopardizing future resin production. Here, we reveal evidence of population collapse of B. papyrifera—now the main source of frankincense—throughout its geographic range. Using inventories of 23 populations consisting of 21,786 trees, growth-ring data from 202 trees and demographic models on the basis of 7,246 trees, we find that over 75% of studied populations lack small trees, natural regeneration has been absent for decades, and projected frankincense production will be halved in 20 yr. These changes are caused by increased human population pressure on Boswellia woodlands through cattle grazing, frequent burns and reckless tapping. A literature review showed that other Boswellia species experience similar threats. Populations can be restored by establishing cattle exclosures and fire-breaks, and by planting trees and tapping trees more carefully. Concerted conservation and restoration efforts are urgently needed to secure the long-term availability of this iconic product.