Auxin and brassinosteroids (BR) are key plant hormones that are involved in the regulation of plant growth fitness. Although there is prominent crosstalk in auxin and BR signaling pathways, its mechanistic understanding is missing. We demonstrate that BR controls auxin responses via PIN-LIKES (PILS)-dependent intracellular auxin transport. Our findings reveal that BR signaling transcriptionally and post-translationally represses the accumulation of PILS proteins at the endoplasmic reticulum, thereby increasing nuclear abundance and signaling of auxin. We demonstrate that this alternative phytohormonal crosstalk mechanism integrates BR signaling into auxin-dependent organ growth rates and likely has widespread importance for plant development.