Alphacoronaviruses are widespread but understudied in comparison to betacoronaviruses. Within the alphacoronaviruses is the species Alphacoronavirus-1, which comprises distinct viruses of cats, dogs and pigs, along with a separate species that infects mustelids—as well other related viruses of pigs and circulating human viruses. High-pathogenicity feline coronavirus (FCoV) is infamous as the cause of feline infectious peritonitis (FIP), existing as two distinct genotypes (type -1 and -2) and transmitted as a low-pathogenicity virus. The high-pathogenicity variants arise in cats infected with FCoV, and while the mutations responsible remain enigmatic, the main determinant is the spike glycoprotein. FCoV-1 disease outcome is driven by a combination of both within- and between-host evolution; virulence can be largely explained by the “internal mutation hypothesis”, which argues that high pathogenicity—but poorly transmissible—variants are selected in individual cats. Canine coronaviruses are generally considered low pathogenicity but can cause severe enteritis and be systemic. Notably the CCoV spike gene periodically recombines with FCoV-1 to generate FCoV-2, which is exemplified by FCoV-23, which has caused a widespread outbreak of FIP in Cyprus and has a notably truncated spike N-terminal domain (NTD). In pigs, coronaviruses often cause severe gastrointestinal disease but can become respiratory and have low pathogenicity based on what can also be considered an ‘internal deletion’ of the spike NTD. These viruses may exist as a dynamic "metavirome"1 that is in a constant state of flux, presenting notable challenges for disease surveillance and management.