In plants, miR390 directs the production of tasiRNAs from TRANS-ACTING SIRNA3 (TAS3) transcripts to regulate AUXIN RESPONSIVE FACTOR (ARF) genes, critical for auxin signaling; these tasiRNAs are known as tasiARFs. To understand the evolution of this miR390-TAS3-ARF pathway, we characterized homologs of these three genes from thousands of plant species, from bryophytes to angiosperms. We found the lower-stem region of MIR390 genes, critical for accurate DICERLIKE1 processing, is conserved in sequence in seed plants. We propose a model for the transition of functional tasiRNA sequences in TAS3 genes occurred at the emergence of vascular plants, in which the two miR390 target sites of TAS3 genes showed distinct pairing patterns. Based on the cleavability of miR390 target sites and the distance between target site and tasiARF, we inferred a potential bidirectional processing mechanism exists for some TAS3 genes. We also demonstrated a tight mutual selection between tasiARF and its target genes and that ARGONAUTE7, the partner of miR390, was specified later than other factors in the pathway. All these data illuminate the evolutionary path of the miR390-TAS3-ARF pathway in land plants and demonstrate the significant variation that occurs in this functionally important and archetypal regulatory circuit.