The Drosophila melanogaster fourth chromosome contains interspersed domains of active and repressive chromatin. We investigated a stock harboring a silenced transgene inserted into Dyrk3 and near Caps-two expressed genes on chromosome four. In an HP1a-deficient background, transgene expression was activated while, paradoxically, expression of Dyrk3 and Caps was reduced. We found that the promoters of Dyrk3 and Caps contained DNase I hypersensitive sites but also possessed methylated histone H3 and HP1a, marks of repressive chromatin. In HP1a-deficient flies, the Dyrk3 and Caps promoters displayed diminished accessibility to nuclease digestion, revealing a surprising role for HP1a in opening chromatin.