For plant viruses a successful infection correlates with the ability to access the vascular phloem and move systemically into distal tissues. However, how viruses gain access to and usurp vascular tissues is poorly understood. Here we show how tobacco mosaic virus (TMV) enhances its access to the phloem of mature plant tissues through the targeted disruption of auxin/indole acetic acid (Aux/IAA) transcriptional regulators that control expression of host genes involved in virus cell-to-cell movement, plasmodesmata gating, and defense. TMV’s ability to disrupt Aux/IAA function successfully confers a significant advantage in the systemic spread of this virus, allowing it to outcompete nondisrupting viruses. In summary, TMV interacts with Aux/IAA proteins to reprogram the vascular phloem, making it more conducive to systemic movement.