Avian wing length is an important trait that covaries with the ecology and migratory behaviour of a species and tends to change rapidly when the conditions are altered. Long-distance migrants typically have longer wings than short-distance migrants and sedentary species, and long-winged species also tend to be more dispersive. Although the substantial heritability of avian wing length is well established, the identification of causal genes has remained elusive. Based on large-scale genotyping of 1404 informative single nucleotide polymorphisms (SNP) in a captive population of 1067 zebra finches, we here show that the within-population variation of relative wing length (h2 = 0.74 ± 0.05) is associated with standing genetic variation in at least six genomic regions (one genome-wide significant and five suggestive). The variance explained by these six quantitative trait loci (QTL) sums to 36.8% of the phenotypic variance (half of the additive genetic variance), although this likely is an overestimate attributable to the Beavis effect. As avian wing length is primarily determined by the length of the primary feathers, we then searched for candidate genes that are related to feather growth. Interestingly, all of the QTL signals co-locate with Wnt growth factors and closely interacting genes (Wnt3a, Wnt5a, Wnt6, Wnt7a, Wnt9a, RhoU and RhoV). Our findings therefore suggest that standing genetic variation in the Wnt genes might be linked to avian wing morphology, although there are many other genes that also fall within the confidence regions.