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The collection of caterpillar fungus accounts for 50–70% of the household income of thousands of Himalayan communities and has an estimated market value of $5–11 billion across Asia. However, Himalayan collectors are at multiple economic disadvantages compared with collectors on the Tibetan plateau because their product is not legally recognized. Using a customized hybrid-enrichment probe set and market-grade caterpillar fungus (with samples up to 30 years old) from 94 production zones across Asia, we uncovered clear geography-based signatures of historical dispersal and significant isolation-by-distance among caterpillar fungus hosts. This high-throughput approach can readily distinguish samples from major production zones with definitive geographical resolution, especially for samples from the Himalayan region that form monophyletic clades in our analysis. Based on these results, we propose a two-step procedure to help local communities authenticate their produce and improve this multi-national trade-route without creating opportunities for illegal exports and other forms of economic exploitation. We argue that policy makers and conservation practitioners must encourage the fair trade of caterpillar fungus in addition to sustainable harvesting to support a trans-boundary conservation effort that is much needed for this natural commodity in the Himalayan region.