RNA polymerase I (Pol I) mediated transcription of the ribosomal RNA genes (rDNA) is frequently upregulated in cancer, including acute myeloid leukemia (AML)1,2. rDNA is highly vulnerable to DNA damage and inhibition of Pol I transcription by a selective inhibitor CX-5461, which is currently in clinical trials, induces a nucleolar-specific DNA damage response (DDR) via ATM/ATR signalling. While single agent CX-5461 provides an impressive survival benefit in preclinical mouse models of AML, animals eventually succumb to disease, underscoring the need for Pol I inhibitor combination therapies1,2. Inhibitors of bromodomain and extra-terminal (BET) proteins, also in clinical trials, block BET protein binding to acetylated chromatin marks and growing evidence has established a role for BET proteins in DDR regulation, via transcriptional regulation and direct effects on chromatin accessibility3,4. Here, we report a striking synergy between CX-5461 and the BET protein inhibitor IBET-151, where their co-treatment significantly improved survival over single agents in preclinical models of aggressive AML. Following treatment of AML cells with IBET-151 or the knockdown of its target BRD4, we demonstrate a dramatic increase in rDNA accessibility to MNase. Significantly, co-treatment of AML cells with IBET-151 and CX-5461 led to a heightened DDR at rDNA chromatin, evidenced by marked γH2AX enrichment at rDNA. Mechanistically, our data demonstrate that inhibition of BRD4 by IBET-151 results in more open rDNA chromatin, exposing the rDNA to enhanced CX-5461-mediated DDR and leading to synthetic lethality of AML cells. Intriguingly, IBET-151-resistant cells5 are re-sensitised to BRD4 inhibition when combined with CX-5461, where co-treatment activated this synergistic ATM-mediated response independent of IBET-151 resistance pathways. Together, these studies highlight the therapeutic value of using BET inhibitors to amplify the underlying sensitivity of rDNA to DNA damage and thus exploit a previously unexplored synthetic lethality between BET protein and Pol I transcription inhibition for treating AML.