Filamentous fungi link morphological differentiation with secondary metabolism. Although disperse genetic evidence correlates both processes with epigenetic activities, a chromatin modification mechanism has been elusive. Here, we describe a tetrameric chromatin modification complex in the filamentous fungus Aspergillus nidulans that is composed of the H3K4 histone demethylase KdmB, a cohesin acetyltransferase (EcoA), a histone deacetylase (RpdA) and a reader protein (SntB). The KERS complex assembles in the nucleus from KdmB-EcoA and RpdA-SntB heterodimers and is found at more than a thousand promoters enriched for morphological differentiation and regulation of secondary metabolites. KERS provides the first mechanistic, chromatin-centered understanding of how fungal reproductive development is connected with small molecule synthesis.