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ABSTRACT Priority effects, where the order and timing of species arrival influence the assembly of ecological communities, have been observed in a variety of taxa and habitats. However, the genetic and molecular basis of priority effects remains unclear, hindering a better understanding of when priority effects will be strong. We sought to gain such an understanding for the nectar yeastMetschnikowia reukaufiicommonly found in the nectar of our study plant, the hummingbird‐pollinatedDiplacus(Mimulus)aurantiacus. In this plant,M.reukaufiican experience strong priority effects when it reaches flowers after other nectar yeasts, such asM.rancensis. After inoculation into two contrasting types of synthetic nectar simulating early arrival ofM.rancensis, we conducted whole‐transcriptome sequencing of 108 strains ofM.reukaufii. We found that several genes were differentially expressed inM.reukaufiistrains when the nectar had been conditioned by growth ofM.rancensis. Many of these genes were associated with amino acid metabolism, suggesting thatM.reukaufiistrains responded molecularly to the reduction in amino acid availability caused byM.rancensis. Furthermore, investigation of expression quantitative trait loci (eQTLs) revealed that genes involved in amino acid transport and resistance to antifungal compounds were enriched in some genetic variants ofM.reukaufii. We also found that gene expression was associated with population growth rate, particularly when amino acids were limited. These results suggest that intraspecific genetic variation in the ability of nectar yeasts to respond to nutrient limitation and direct fungal competition underpins priority effects in this microbial system.