Douglas-fir (Pseudotsuga menziesii) is a conifer tree native to western North America. In central Europe, it shows superior growth performance and is considered a suitable substitute for tree species impaired in vitality due to climate change. Maintenance and improvement of growth performance in a changing environment is a main challenge for forest tree breeders. In this context, genetic variation as a factor underlying phenotypic variation, but also as the basis for future adaptation, is of particular interest. The aims of this study were to analyse (i) genetic diversity of selected Douglas-fir provenances, (ii) variation in height growth among provenances, and (iii) to assess the link between genetic and phenotypic variation height growth. Genotyping was done on microsatellite loci. Effects of provenance, genotype, and site on height growth were assessed by fitting mixed linear models. The most significant genetic differentiation was observed between provenances of the coastal variety, versus a provenance of the interior variety originating from British Columbia. Although genetic differentiation among provenances of the coastal variety was lower, genetic structures within this variety were identified. Moreover, genetic diversity showed a latitudinal gradient with the southernmost provenances being more diverse, probably reflecting the species’ evolutionary history. The modelling approach revealed that height growth differed significantly by provenance, site, and the interaction between site and provenance, demonstrating that height growth is under strong genetic control. Additionally, this analysis showed that genetic variation captured by the genotyped microsatellite loci was significantly related to variation in height growth, providing statistical evidence for a genetic component in the observed phenotypic variation.