Heterochromatin formation is generally thought to result in transcriptional repression of target loci. However, RNAi-mediated heterochromatin assembly requires RNA polymerase II (Pol II) transcription. The mechanism facilitating Pol II accessibility to heterochromatin is unknown. We show that the fission yeast Epe1, a JmjC domain-containing protein and a negative regulator of heterochromatin, is distributed across all major heterochromatic domains and at certain meiotic genes. Remarkably, Epe1 is recruited to heterochromatic loci by the heterochromatin protein Swi6/HP1. Moreover, Epe1 acts in a heterochromatin-specific context to promote Pol II accessibility by counteracting repressive chromatin. This requires Epe1's JmjC domain, although the mechanism utilized might be distinct from other JmjC proteins that possess known demethylase activities. We also find that Epe1 is preferentially recruited to inverted repeats flanking centromeres to restrain the spread of pericentromeric heterochromatin. Our analyses suggest that Swi6/HP1 recruits opposing chromatin-modifying activities, the balancing of which is crucial for heterochromatin maintenance.