Mountains form a diverse mosaic of microhabitats over small distances created by changes in climate, soil, and water availability. A key to adaptation of plants to such microhabitats is genetic variation; however, natural accumulation of genetic variation through mutation is slow and often not sufficient alone. Adaptive introgression via hybridization is an alternative to generate genetic variation. Here, we investigate hybridization and discuss its adaptive role in Veronica subg. Pseudolysimachium at their Altai Mountains distribution. To support our hypotheses of frequent hybridization, we genotyped thousands of SNPs for 233 individuals from 10 species and 7 putative hybrids previously described based on morphology. We employed Bayesian and likelihood statistical models and supported our results by morphometric analysis and genomic in situ hybridization (GISH). The results suggest that almost all the individuals of the putative hybrids are of F1 type. The GISH investigation in one case strongly supports homoploid hybridization (origin of V. ×schmakovii from V. longifolia and V. porphyriana. Divergence times of Altai Veronica species are estimated to be within 1–2 million years ago with high probability of gene flow over that time. Our results also demonstrate that the direction of gene flow is mainly from the locally endemic V. porphyriana. We hypothesize that the large Siberian plains and topographically diverse foreland of the Altai Mountains provide an ideal setting for hybridization with the potential for adaptive introgression of alleles conferring tolerance to cooler climates, to the lowland species migrating into the Altai Mountains.