Agrobacterium has evolved sophisticated strategies to perceive and transduce plant‐derived cues. Recent studies have found that numerous plant signals, including salicylic acid (SA), indole‐3‐acetic acid (IAA) and γ‐amino butyric acid (GABA), profoundly affect Agrobacterium–plant interactions. Here we determine and compare the transcriptome profiles of Agrobacterium in response to these three plant signals. Collectively, the transcription of 103, 115 and 95 genes was significantly altered by SA, IAA and GABA respectively. Both distinct cellular responses and overlapping signalling pathways were elicited by these three plant signals. Interestingly, these three plant compounds function additively to shut off the Agrobacterium virulence programme and activate the quorum‐quenching machinery. Moreover, the repression of the virulence programme by SA and IAA and the inactivation of quorum‐sensing signals by SA and GABA are regulated through independent pathways. Our data indicate that these plant signals, while cross‐talk in plant signalling networks, also act as cross‐kingdom signals and play redundant roles in tailoring Agrobacterium regulatory pathways, resulting in intensive signalling cross‐talk in Agrobacterium. Our results support the notion that Agrobacterium has evolved the ability to hijack plant signals for its own benefit. The complex signalling interplay between Agrobacterium and its plant hosts reflects an exquisite co‐evolutionary balance.