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Veronica subgenus Pentasepalae is the largest subgenus of Veronica in the Northern Hemisphere with approximately 80 species mainly from Southwest Asia. In order to reconstruct the phylogenetic relationships among the members of V. subgenus Pentasepalae and to test the “out of the Iranian plateau” hypothesis, we applied thorough taxonomic sampling, employing nuclear DNA (ITS) sequence data complimented with morphological studies and chromosome number counts. Several high or moderately supported clades are reconstructed, but the backbone of the phylogenetic tree is generally unresolved, and many Southwest Asian species are scattered along a large polytomy. It is proposed that rapid diversification of the Irano-Turanian species in allopatric glacial refugia and a relatively high rate of extinction during interglacial periods resulted in such phylogenetic topology. The highly variable Asian V. orientalis–V. multifida complex formed a highly polyphyletic assemblage, emphasizing the idea of cryptic speciation within this group. The phylogenetic results allow the re-assignment of two species into this subgenus. In addition, V. bombycina subsp. bolkardaghensis, V. macrostachya subsp. schizostegia and V. fuhsii var. linearis are raised to species rank and the new name V. parsana is proposed for the latter. Molecular dating and ancestral area reconstructions indicate a divergence age of about 9 million years ago and a place of origin on the Iranian Plateau. Migration to the Western Mediterranean region has likely taken place through a North African route during early quaternary glacial times. This study supports the assumption of the Irano-Turanian region as a source of taxa for neighboring regions, particularly in the alpine flora.