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Closely-related species often use the same genes to adapt to similar environments 1, 2. However, we know little about why such genes possess increased adaptive potential, and whether this is conserved across deeper evolutionary time. Classic theory suggests a “cost of complexity”: adaptation should occur via genes affecting fewer traits to reduce deleterious side-effects (ie lower pleiotropy) 3. Adaptation to climate presents a natural laboratory to test this theory, as even distantly-related species must contend with similar stresses 4. Here, we re-analyse genomic data from thousands of individuals from 25 plant species to identify a suite of 108 genes enriched for signatures of repeated local adaptation to climate. This set includes many genes with well-known functions in abiotic stress response, identifying key genes that repeatedly drive adaptation in species as distantly-related as lodgepole pine and Arabidopsis (~ 300 My). Using gene co-expression networks to quantify each gene’s pleiotropy, we find enrichment for greater network centrality/interaction strength and broader expression across tissues (ie higher pleiotropy), contrary to the” cost of complexity” theory. These genes may be particularly important in helping both wild and crop species cope with future climate change, representing a set of important candidates for future study.