Flooding events negatively affect plant performance and survival. Flooding gradients thereby determine dynamics in vegetation composition and species abundance. In adaptation to flooding, the group VII Ethylene Response Factor genes (ERF-VIIs) play pivotal roles in rice and Arabidopsis through regulation of anaerobic gene expression and antithetical survival strategies. We investigated if ERF-VIIs have a similar role in mediating survival strategies in eudicot species from flood-prone environments. Here we studied the evolutionary origin and regulation of ERF-VII transcript abundance, and the physiological responses in species from two genera of divergent taxonomic lineages (Rumex and Rorippa). Synteny analysis revealed that angiosperm ERF-VIIs arose from two ancestral loci and that subsequent diversification and duplication(s) led to the present ERF-VII variation. We propose that subtle variation in the regulation of ERF-VII transcript abundance could explain variation in tolerance amongst Rorippa species. In Rumex, the main difference in flood tolerance correlated with genetic variation in ERF-VII genes. Large transcriptional differences were found by comparing the two genera: darkness and dark submergence induced Rumex ERF-VIIs, whereas HRE2 expression was increased in submerged Rorippa roots. We conclude that the involvement of ERF-VIIs in flooding tolerance developed in a phylogenetic dependent manner, with subtle variations within taxonomic clades.