Licensee MDPI, Basel, Switzerland. The recent discovery of novel alphacoronaviruses (alpha-Co. Vs) in European and Asian rodents revealed that rodent coronaviruses (Co. Vs) sampled worldwide formed a discrete phylogenetic group within this genus. To determine the evolutionary history of rodent Co. Vs in more detail, particularly the relative frequencies of virus-host co-divergence and cross-species transmission, we recovered longer fragments of CoV genomes from previously discovered European rodent alpha-Co. Vs using a combination of PCR and high-throughput sequencing. Accordingly, the full genome sequence was retrieved from the UK rat coronavirus, along with partial genome sequences from the UK field vole and Poland-resident bank vole Co. Vs, and a short conserved ORF1b fragment from the French rabbit CoV. Genome and phylogenetic analysis showed that despite their diverse geographic origins, all rodent alpha-Co. Vs formed a single monophyletic group and shared similar features, such as the same gene constellations, a recombinant beta-CoV spike gene, and similar core transcriptional regulatory sequences (TRS). These data suggest that all rodent alpha Co. Vs sampled so far originate from a single common ancestor, and that there has likely been a long-term association between alpha Co. Vs and rodents. Despite this likely antiquity, the phylogenetic pattern of the alpha-Co. Vs was also suggestive of relatively frequent host-jumping among the different rodent species.