Copy number variation (CNV) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on a tRNA ligase gene (RLG1a) exhibiting unprecedented, and fitness-relevant, CNV within an annual population of the yellow monkeyflower Mimulus guttatus. Variation at RLG1a was associated with multiple traits in pooled population resequencing (PoolSeq) scans of phenotypic and phenological cohorts. Five of 35 (14%) of resequenced inbred lines carried three-copy variants of RLG1a (trip+), and trip+ lines exhibited elevated RLG1a expression. trip+ carriers, in addition to being over-represented in late-flowering and large-flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (P < 0.05). In early-flowering wild cohorts, we discovered an additional rare variant (high+) that carries 250-300 copies of RLG1a totaling ~5.7Mb, equivalent to 20-40% of a chromosome. Mendelian segregation of diagnostic alleles and qPCR-based copy counts In the progeny of a high+ carrier, indicate that high+ is a single tandem array unlinked from the single copy RLG1a locus in the reference genome. In the wild, high+ carriers had highest fitness in two dry and/or hot years (2015 and 2017; both P < 0.01), while single copy individuals were twice as fecund as either CNV genotype in a lush year (2016: p < 0.005). Our results demonstrate fluctuating selection on CNVs affecting phenological traits in a wild population, suggest that plant tRNA ligases mediate stress-responsive life-history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification.