European beech (Fagus sylvatica L.) is one of the most important forest tree species in Europe, and its genetic adaptation potential to climate change is of great interest. Saplings and adults from 12 European beech populations were sampled along two steep precipitation gradients in Switzerland. All individuals were genotyped at 13 microsatellite or simple sequence repeat (SSR) markers and 70 single nucleotide polymorphisms (SNPs) in 24 candidate genes potentially involved in stress response and phenology. Both SSR and SNP markers revealed high genetic diversity in the studied populations and low but statistically significant population differentiation. The SNPs were searched for F-ST outliers using three different methods implemented in LOSITAN, Arlequin, and BayeScan, respectively. Additionally, associations of the SNPs with environmental variables were tested by two methods implemented in Bayenv2 and Samada, respectively. There were 14 (20%) SNPs in 12 (50%) candidate genes in the saplings and 9 (12.8%) SNPs in 7 (29.2%) candidate genes in the adults consistently identified by at least two of the five methods used, indicating that they are very likely under selection. Genes with SNPs showing signatures of selection are involved in a wide range of molecular functions, such as oxidoreductases (IDH), hydrolases (CysPro), transferases (XTH), transporters (KT2), chaperones (CP10), and transcription factors (DAG, NAC transcription factor). The obtained data will help us better understand the genetic variation underlying adaptation to environmentally changing conditions in European beech, which is of great importance for the development of scientific guidelines for the sustainable management and conservation of this important species.