A dominant dwarfing gene, ds - 4 , encodes an Aux/IAA protein that negatively regulates plant stature through an auxin signaling pathway. Dwarfism is an important agronomic trait affecting yield in many crop species. The molecular mechanisms underlying dwarfism in oilseed rape (Brassica napus) are poorly understood, restricting the progress of breeding dwarf varieties in this species. Here, we identified and characterized a new dwarf locus, DS-4, in B. napus. Next-generation sequencing-assisted genetic mapping and candidate gene analysis found that DS-4 encodes a nucleus-targeted auxin/indole-3-acetic acid (Aux/IAA) protein. A substitution (P87L) was found in the highly conserved degron motif of the Aux/IAA7 protein in the ds-4 mutant. This mutation co-segregated with the phenotype of individuals in the BC1F2 population. The P87L substitution was confirmed as the cause of the extreme dwarf phenotype by ectopic expression of the mutant allele BnaC05.iaa7 (equivalent to ds-4) in Arabidopsis. The P87L substitution blocked the interaction of BnaC05.iaa7 with TRANSPORT INHIBITOR RESPONSE 1 in the presence of auxin. The BnaC05.IAA7 gene is highly expressed in the cotyledons, hypocotyls, stems and leaves, but weakly in the roots and seeds of B. napus. Our findings provide new insights into the molecular mechanisms underlying dominant (gain-of-function) dwarfism in B. napus. Our identification of a distinct gene locus controlling plant height may help to improve lodging resistance in oilseed rape.