SummaryAuxin/indole acetic acid (Aux/IAA) proteins regulate transcriptional responses to the plant hormone auxin. Gain‐of‐function mutations in the Arabidopsis SHORT HYPOCOTYL 2 (SHY2/IAA3) gene encoding an Aux/IAA protein increase steady‐state levels of SHY2/IAA3 protein and decrease auxin responses, indicating that SHY2/IAA3 negatively regulates auxin signaling. These shy2 mutations also cause ectopic light responses, suggesting that SHY2/IAA3 may promote light signaling. Auxin regulates turnover of the related Auxin‐resistant (AXR)2/IAA7 and AXR3/IAA17 proteins by increasing their interaction with the Skp1‐Cdc53/cullin‐F‐box (SCFTIR1) E3 ubiquitin ligase complex. To investigate whether SHY2/IAA3 is regulated similarly, we have used a turnover assay to reveal that axr1 and transport inhibitor resistant (tir)1 mutations affecting SCFTIR1 decrease SHY2/IAA3 turnover. In pull‐down assays, SHY2/IAA3 protein interacted with TIR1, the F‐box component of SCFTIR1 and with the photoreceptor phytochrome B. Auxin stimulated SHY2/IAA3 interaction with TIR1, whereas the shy2‐2 gain‐of‐function mutation decreased this interaction. Light did not affect the interaction, suggesting that light regulates some other aspect of Aux/IAA gene or protein function. The chemical juglone (5‐hydroxy‐1,4‐naphthoquinone) inhibited the interaction, suggesting that peptidyl‐prolyl isomerization may mediate auxin‐induced SHY2/IAA3 protein turnover.