DELLA proteins are land-plant specific transcriptional regulators that transduce environmental information to multiple processes throughout a plant's life. The molecular basis for this critical function in angiosperms has been linked to the regulation of DELLA stability by gibberellins and to the capacity of DELLA proteins to interact with hundreds of transcription factors. Although bryophyte orthologues can partially fulfil functions attributed to angiosperm DELLA, it is not clear whether the capacity to establish interaction networks is an ancestral property of DELLA proteins or is associated with their role in gibberellin signalling. Here we show that representative DELLAs from the main plant lineages display a conserved ability to interact with multiple transcription factors. We propose that promiscuity was encoded in the ancestral DELLA protein, and that this property has been largely maintained, whereas the lineage-dependent diversification of DELLA-dependent functions mostly reflects the functional evolution of their interacting partners.