The interplay between vascular development and leaf development is central to the evolutionary success of vascular plants, yet the underlying mechanisms remain poorly understood. Here, we identify the RNA-binding protein JULGI1 (JUL1) as a key integrator of vascular and leaf development in Arabidopsis. JUL1 is transcribed in leaf veins, while the protein distributes throughout the leaf, where it binds G-rich regions of pri-MIR165a transcripts on the abaxial side. This interaction disrupts hairpin formation and inhibits DICER-LIKE1 (DCL1)-mediated processing, reducing miR165/166 levels. Consequently, transcript levels of their targets, the Class III homeodomain leucine zipper (HD-ZIP III), increase, reinforcing adaxial-abaxial polarity. Our findings reveal a non-cell-autonomous mechanism by which vascular-derived JUL1 modulates miRNA biogenesis to coordinate leaf patterning with vascular development.