Flowering time is an adaptive life history trait. Capsella rubella, a close relative of Arabidopsis thaliana and a young species, displays extensive variation for flowering time but low standing genetic variation due to an extreme bottleneck event, providing an excellent opportunity to understand how phenotypic diversity can occur with a limited initial gene pool. Here, we demonstrate that common allelic variation and parallel evolution at the FLC locus confer variation in flowering time in C. rubella. We show that two overlapping deletions in the 5′ untranslated region (UTR) of C. rubella FLC, which are associated with local changes in chromatin conformation and histone modifications, reduce its expression levels and promote flowering. We further show that these two pervasive variants originated independently in natural C. rubella populations after speciation and spread to an intermediate frequency, suggesting a role of this parallel cis-regulatory change in adaptive evolution. Our results provide an example of how parallel mutations in the same 5′ UTR region can shape phenotypic evolution in plants.