Competition between genotypes within a plant population can result in the displacement of the least competitive by more competitive genotypes. Although evolutionary processes in plants may occur over thousands and millions of years, it has been suggested that changes in key fitness traits could occur in as little as decades, with herbicide resistance being a common example. However, the rapid evolution of complex traits has not been proven in weeds. We hypothesized that changes in weed growth and competitive ability can occur in just a few years because of selection in agroecosystems. Seed of multiple generations of a single natural population of the grassy weed giant foxtail (Setaria faberi Herrm.) were collected during 34 yr (i.e., 1983 to 2017). Using a “resurrection” approach, we characterized life-history traits of the different year-lines under noncompetitive and competitive conditions. Replacement-series experiments comparing the growth of the oldest year-line (1983) versus newer year-lines (1991, 1996, 1998, 2009, and 2017) showed that plant competitive ability decreased and then increased progressively in accordance with oscillating selection. The adaptations in competitive ability were reflected in dynamic changes in leaf area and biomass when plants were in competition. The onset of increased competitive ability coincided with the introduction of herbicide-resistant crops in the landscape in 1996. We also conducted a genome-wide association study and identified four loci that were associated with increased competitive ability over time, confirming that this trait changed in response to directional selection. Putative transcription factors and cell wall–associated enzymes were linked to those loci. This is the first study providing direct in situ evidence of rapid directional evolution of competitive ability in a plant species. The results suggest that agricultural systems can exert enough pressure to cause evolutionary adaptations of complex life-history traits, potentially increasing weediness and invasiveness.