Significance How chromatin influences transcription is a major question in biology. Chromatin states and transcriptional activity are correlated, but the interconnections and feedbacks in chromatin regulation that lead to quantitative transcriptional regulation are poorly understood. Previous mathematical modeling has shown the importance of dynamic, opposing histone modifications to enable maintenance of one chromatin state through many cell divisions, yet retain the ability to switch from one state to the other. Here, we validate a prediction of that modeling—physical association between the histone modifiers: the methyltransferase specific for the active state with the demethylase specific for the silent state. Such physical coupling of activities regulating opposing chromatin states is likely to be a general feature in chromatin-based transcriptional regulation.