Relating molecular variation to phenotypic diversity is a major goal in evolutionary biology. In Arabidopsis thaliana, FLOWERING LOCUS C (FLC) is a major determinant of the variation in vernalization- the acceleration of flowering by prolonged cold. Here, we analyse the worldwide FLC haplotype structure and identify five predominant FLC haplotypes defined by non-coding sequence variation. Genetic and transgenic experiments show they are functionally distinct with non-coding polymorphism influencing the rate of FLC epigenetic silencing. This non-coding variation at a single locus accounts for a large proportion of natural variation in vernalization of A. thaliana accessions. These multiple, functionally distinct FLC haplotypes appear to contribute to the broad geographical range of A. thaliana accessions.