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ABSTRACT As environments worldwide change at unprecedented rates during the Anthropocene, understanding context dependency—how species interactions vary depending on environmental context—is crucial. Combining comparative genomics across 42 angiosperms with transcriptomics, genome‐wide association mapping and gene duplication origin analyses, we show for the first time that gene family expansions are important to context‐dependent regulation of species interactions. Gene families expanded in mycorrhizal fungi‐associating plants display up to 200% more context‐dependent gene expression and double the genetic variation associated with mycorrhizal benefits to plant fitness. Moreover, we discover these gene family expansions arise primarily from tandem duplications with > 2‐times more tandem duplications genome‐wide, indicating gene family expansions continuously supply genetic variation, allowing fine‐tuning of context dependency in species interactions throughout plant evolution. Taken together, our results spotlight how widespread gene duplications can provide molecular flexibility required for plant–microbial interactions to match changing environmental conditions.