The role of second messengers in mediating virulence has been well-established in different bacterial pathogens. However, despite Acinetobacter baumannii being the top critical-priority pathogen, its regulation of virulence-related phenotypes by these signalling systems is elusive. In this work, we used high-throughput screening of the A. baumannii AB5075 transposon mutant library to identify novel biofilm formation regulators. A clean deletion mutant of the candidate gene was created and we analysed its effect on the transcriptome using dRNA-Seq. Subsequently, the transcriptomic results were phenotypically validated. We identified a previously uncharacterised predicted adenylate cyclase (AC), CavA, as a central regulator in A. baumannii. CavA was confirmed to be a functional AC synthesizing cAMP. Uncovering the CavA-mediated cAMP regulon showed that cAMP upregulated type IV pili while downregulating Csu pili and exopolysaccharide production genes transcription. In addition, we provide evidence that Vfr function is cAMP-dependent. We demonstrate for the first time that, cAMP is atop of a hierarchical signalling cascade. It controls inter- and intrabacterial signalling by modulating quorum sensing and c-di-GMP systems at transcriptional level, ultimately governing virulence in vivo and adaptive antibiotic resistance in A. baumannii. We challenge the established norm of high c-di-GMP leading to increased biofilm formation, as our results show that this paradigm is dependent on intracellular cAMP concentrations in A. baumannii. Overall, we demonstrate the central role of cAMP in modulating key virulence related phenotypes and suggest a possible hierarchy of the signalling systems in A. baumannii. This highlights cAMP as a potential target for novel therapeutic development.