Remarkably stable genomic chromosome elements (evolutionary conserved segments or syntenies) are the basis of large-scale chromosome architecture in vertebrate species. However, these syntenic elements harbour evolutionary important changes through intrachromosomal rearrangements such as inversions and centromere repositioning. Here, using FISH with a set of 20 region-specific probes on a wide array of 28 species, we analyzed evolution of three conserved syntenic regions of the Arvicolinae ancestral karyotype. Inside these syntenies we uncovered multiple, previously cryptic intrachromosomal rearrangements. Although in each of the three conserved blocks we found inversions and centromere repositions, the blocks experienced different types of rearrangements. In two syntenies centromere repositioning predominated, while in the third region, paracentric inversions were more frequent, whereas pericentric inversions were not detected. We found that some of the intrachromosomal rearrangements, mainly paracentric inversions, were synapomorphic for whole arvicoline genera or tribes: genera Alexandromys and Microtus, tribes Ellobini and Myodini. We hypothesize that intrachromosomal rearrangements within conserved syntenic blocks are a major evolutionary force modulating genome architecture in species-rich and rapidly-evolving rodent taxa. Inversions and centromere repositioning may impact speciation and provide a potential link between genome evolution, speciation, and biogeography.