Sugar beet is a biennial plant with an absolute requirement of vernalization, corresponding to the acquisition of the competence to bolt and flower after a prolonged exposure to low temperatures. The cold duration needed to induce bolting and flowering varies depending on the genotypes, reflecting their bolting tolerance, which is an essential agronomic trait. This work aimed at (i) investigating a possible epigenetic control of bolting induction in bolting sensitive and bolting resistant sugar beet genotypes, (ii) identifying sequences targeted by DNA methylation and expression remodeling, and (iii) characterizing candidate sequences which could be used in marked-assisted selection for plant breeding. Our data suggest that the time course and amplitude of DNA methylation variations are critical points for the induction of sugar beet bolting and represent an epigenetic component of the genotypic bolting tolerance. In addition, we identified differentially methylated sequences exhibiting variations of gene-body DNA methylation and expression during cold exposure and/or between genotypes. Among them, two RNA METHYLCYTOSINE TRANSFERASES, in association with RNA methylation such as BvFL1 mRNA, a floral repressor, were shown to play a role in floral transition. Finally, using microarrays we identified an integrative network of genes including response to environment, phytohormone signalling and flowering induction. The activation kinetics of these genes could define the bolting tolerance level of sugar beet genotypes.