Drought stress, especially at the reproductive stage, is a major limiting factor that compromises the productivity and profitability of canola in many regions of the world. Improved genetics for drought tolerance would enable the identification and development of resilient cultivars, resulting in increased canola production. The main objective of the present study was to dissect the genetic basis of seed yield of canola under water-limited conditions. A doubled haploid population derived from a cross between two Australian parental lines, RP04 and Ag-Outback, was evaluated to identify the genetic variation in fractional normalised deviation vegetative index (NDVI), aboveground shoot biomass accumulation, flowering time and plasticity in seed yield under irrigated and rainfed field conditions in two consecutive years. An irrigation treatment was applied at the 50% flowering stage and an incremental drought tolerance index (DTI) was estimated for seed yield. By utilising a genetic linkage map based on 18 851 genome-wide DArTseq markers, we identified 25 genomic regions significantly associated with different traits (logarithm of odds (LOD) ≥ 3), accounting for 5.5–22.3% of the genotypic variance. Three significant genomic regions on chromosomes A06, A10 and C04 were associated with DTI for seed yield. Some of the quantitative trait loci (QTL) were localised in the close proximity of candidate genes involved in traits contributing to drought escape and drought avoidance mechanisms, including FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC). Trait-marker associations identified herein can be validated across diverse environments, and the sequence-based markers may be used in a marker assisted selection breeding strategy to enhance drought tolerance in canola breeding germplasm.