The development of multicellular organisms relies on interconnected genetic programs that control progression through their life cycle. MicroRNAs (miRNAs) and transcription factors (TFs) play key roles in such regulatory circuits. Here, we describe how three evolutionary conserved miRNA-TF pairs interact to form multiple checkpoints during reproductive development of Arabidopsis thaliana. Genetic, cellular, and physiological experiments show that miR159- and miR319-regulated MYB and TCP transcription factors pattern the expression of miR167 family members and their ARF6/8 targets. Coordinated action of these miRNA-TF pairs is crucial for the execution of consecutive hormone-dependent transitions during flower maturation. Cross-regulation includes both cis- and trans-regulatory interactions between these miRNAs and their targets. Our observations reveal how different miRNA-TF pairs can be organized into modules that coordinate successive steps in the plant life cycle.