Novel developmental programs often evolve via the cooption of existing genetic networks. To gain insight into this evolutionary process, we explored an independent cooption event of the TAS3 tasiRNA pathway, which has been repeatedly redeployed over the course of plant evolution, in the moss Physcomitrella patens. We find an ancestral role for this pathway in the spatial regulation of a conserved set of Auxin Response Factors. In moss, this results in stochastic patterning of the filamentous protonemal tissue. Through a combination of computational modeling and experimentation, we demonstrate that tasiRNA regulation confers sensitivity and robustness onto the auxin response. The loss of auxin sensitivity is paralleled by decreased developmental sensitivity to nitrogen, a key environmental signal. We propose that the properties lent to the auxin response gene regulatory network by tasiRNAs, along with their ability to stochastically modulate development in response to environmental cues, have contributed to the tasiRNA-ARF module’s repeated cooption over the course of plant evolution.