Embryonic genes that regulate normal development are often re-expressed in cancers, yet the functional and molecular consequences of this phenomenon are poorly understood. The epigenetic priming factors Developmental Pluripotency Associated 2 and 4 (DPPA2&4) play crucial roles in early development and are implicated in cancer pathogenesis. We revealed co-expression of DPPA2&4 is associated with poorly differentiated tumours and impaired patient survival in non-small cell lung cancer (NSCLC) subtypes. Consistently, overexpression of DPPA2&4 in human NSCLC cells demonstrated accelerated in vivo xenograft tumour growth. Through proteomic analyses (IP/RIME-MS, EMSA), we found that DPPA2&4 heterodimerise to enhance their protein stability and binding efficiency to nucleosomes. Through multi-omic epigenome profiling (ChIP, CUT&Run, ATAC-seq, BS-seq) and transcriptome analyses (RNA-seq) we found DPPA2&4 associated with and promote active chromatin states in NSCLC. Depleting DPPA2&4 in these NSCLC cells, uncovered a function for DPPA2&4 in maintaining the PRC1 complex (RING1B) and it’s product H2AK119ub at active promoters and enhancers. Surprisingly, these DPPA2&4 regulated H2AK119ub domains lacked detectable repressive H3K27me3 (deposited by the PRC2 complex), despite the presence of the PRC2 complex at some of these sites. Ablation of H3K27ac (deposited by p300/CBP) at these regions using the p300/CBP inhibitor A-485 revealed that DPPA2&4 regulated genes were primed for repression upon H3K27ac removal, elucidating a novel gene poising mechanism. Our results support a model by which DPPA2&4 act as amplifiers of active chromatin states, facilitating the binding and/or activity of chromatin regulators at these domains and ultimately facilitating the detrimental outcomes seen in patients with DPPA2&4 expressing cancers. Our study reveals how aberrant expression of embryonic chromatin regulators in cancers can facilitate alternate chromatin states to regulate gene expression in aggressive tumours.