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Leaf trichomes protect against various biotic and abiotic stresses in plants. However, there is little knowledge about this trait in oilseed rape (Brassica napus). Here, we demonstrated that hairy leaves were less attractive to Plutella xylostella larvae than glabrous leaves. We established a core germplasm collection with 290 accessions for a genome‐wide association study (GWAS) of the leaf trichome trait in oilseed rape. We compared the transcriptomes of the shoot apical meristem (SAM) between hairy‐ and glabrous‐leaf genotypes to narrow down the candidate genes identified by GWAS. The single nucleotide polymorphisms and the different transcript levels of BnaA.GL1.a, BnaC.SWEET4.a, BnaC.WAT1.a and BnaC.WAT1.b corresponded to the divergence of the hairy‐ and glabrous‐leaf phenotypes, indicating the role of sugar and/or auxin signalling in leaf trichome initiation. The hairy‐leaf SAMs had lower glucose and sucrose contents but higher expression of putative auxin responsive factors than the glabrous‐leaf SAMs. Spraying of exogenous auxin (8 μm) increased leaf trichome number in certain genotypes, whereas spraying of sucrose (1%) plus glucose (6%) slightly repressed leaf trichome initiation. These data contribute to the existing knowledge about the genetic control of leaf trichomes and would assist breeding towards the desired leaf surface type in oilseed rape. Our genome‐wide association study in oilseed rape identified new genes, such as BnaA.GL1.a, BnaC.SWEET4.a, BnaC.WAT1.a and BnaC.WAT1.b, that associate with leaf trichome formation, indicating the role of sugar and auxin signalling in leaf trichome initiation of oilseed rape. [ABSTRACT FROM AUTHOR]