Transcriptional regulation in Chlamydiae is still poorly understood. The absence until recently of genetic tools is the main cause of this gap. We discovered three new potential DNA-associated proteins of Waddlia chondrophila, a Chlamydia-related bacterium, using heparin chromatography coupled to mass spectrometry (Wcw_0377, Wcw_1456, and Wcw_1460). By ChIP-seq analysis, we determined the regulatory landscape of these three proteins and we showed that Wcw_0377 binds all along the genome whereas Wcw_1456 and _1460 possess a wide regulon with a large number of co-regulated genes. Wcw_1456 and Wcw_1460 interact with RpoD (σ66), emerging as potential RpoD regulators. On the other hand, Wcw_0377 is able to reach the host nucleus, where it might interact with eukaryotic histones through its putative chromatin-remodelling SWIB/MDM2 domain.