Post-translational modifications of histone tails are an important factor regulating chromatin structure and gene expression. Epigenetic memory systems have been predicted to involve mutually exclusive histone modifications that through positive feedback mechanisms generate bistable states. How the states are interconverted is not understood and whether the histone modifications are sufficient for epigenetic memory is still greatly debated. We have exploited the process of vernalization, the slow quantitative epigenetic silencing of Arabidopsis FLC induced by cold, to detail with fine temporal and spatial resolution the dynamics of histone modifications during an epigenetic switch. The profiles of H3K36me3, H3K4me3 and H3K4me2 at FLC throughout the vernalization process were compared to H3K27me3, which accumulates at a local nucleation region during the cold and spreads across the locus on return to the warm. We find for many phases of the vernalization process H3K36me3 and H3K27me3 show opposing profiles in the FLC nucleation region and gene body, that H3K36me3 and H3K27me3 rarely co-exist on the same histone tail, and that this antagonism is functionally important. A lack of H3K36me3 results in a fully silenced state at FLC even in the absence of cold. We therefore propose that H3K36me3 is the opposing modification to H3K27me3 in the Polycomb-mediated silencing of FLC. However, the lack of an absolute mirror profile predicted from modelling suggests their antagonistic roles contribute a necessary but not sufficient component of the mechanism enabling switching between, and inheritance of, epigenetic states.