Mangroves are adapted to intertidal zones, which present extreme environmental conditions. WRKYs are among the most prominent transcription factors (TFs) in higher plants and act through various interconnected networks to regulate responses to multiple abiotic stressors. Here, based on omic data, we investigated the landscape and evolutionary patterns of WRKYs in the main mangrove genusAvicennia. We found that both the number and the proportion of TFs and WRKYs inAvicenniaspecies exceeded their inland relatives, indicating a significant expansion of WRKYs inAvicennia. We identified 109WRKYgenes in the representative speciesAvicennia marina. Comparative genomic analysis showed that two recent whole-genome duplication (WGD) events played a critical role in the expansion ofWRKYs, and 88% ofAvicennia marina WRKYs (AmWRKYs) have been retained following these WGDs. Applying comparative transcriptomics on roots under experimental salt gradients, we inferred that there is high divergence in the expression of WGD-retainedAmWRKYs. Moreover, we found that the expression of 16AmWRKYs was stable between freshwater and moderately saline water but increased when the trees were exposed to high salinity. In particular, 14 duplicates were retained following the two recent WGD events, indicating potential neo- and sub-functionalization. We also found that WRKYs could interact with other upregulated genes involved in signalling pathways and natural antioxidant biosynthesis to enhance salt tolerance, contributing to the adaptation to intertidal zones. Our omic data of the WRKY family inA. marinabroadens the understanding of how a TF family relates to the adaptive evolution of mangroves.Supplementary InformationThe online version contains supplementary material available at 10.1007/s42995-023-00177-y.