Summary Parallel evolution of the same, or at least very similar, phenotype(s) in different lineages is often interpreted as evidence for the action of natural selection. However, caution is required when inferring parallel evolution based on uncertain or potentially incorrect phylogenetic frameworks. Here, by conducting extensive phylogenomic and population genetic analyses, we aim to clarify the evolutionary history of spurless taxa within the Aquilegia ecalcarata complex. We observed substantial discordance in the phylogenetic patterns across the entire genome, primarily attributed to ancient introgression and incomplete lineage sorting. Additionally, we identified several spurless lineages whose phylogenetic positions were distorted by admixture events. Using a backbone tree and demographic modeling, we determined that these spurless taxa independently originated twice within this group. Intriguingly, our investigation revealed that the spurless taxa experienced population expansion during global cooling, while their spurred sister groups underwent population contraction. The parallel losses of petal spurs, therefore, may be linked to adaptations for low‐temperature conditions. These findings emphasize the importance of comprehensive population‐level analyses in phylogenetic inference and provide valuable insights into the dynamics of trait loss and its implications for the adaptive strategies.