Community protective immunity can affect RNA virus evolution by selecting for new antigenic variants on the scale of years, exemplified by the need of annual evaluation of influenza vaccines . The extent to which this process termed antigenic drift affects coronaviruses remains unknown . Alike the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), seasonal human coronaviruses (HCoV) likely emerged from animal reservoirs as new human pathogens in the past . We therefore analyzed the long-term evolutionary dynamics of the ubiquitous HCoV-229E and HCoV-OC43 in comparison with human influenza A virus (IAV) subtype H3N2 . We focus on viral glycoprotein genes that mediate viral entry into cells and are major targets of host neutralizing antibody responses . Maximum likelihood and Bayesian phylogenies of publicly available gene datasets representing about three decades of HCoV and IAV evolution showed that all viruses had similar ladder-like tree shapes compatible with antigenic drift, supported by different tree shape statistics . Evolutionary rates inferred in a Bayesian framework were 6.5 × 10 -4 (95% highest posterior density (HPD), 5.4-7.5 × 10 -4) substitutions per site per year (s/s/y) for HCoV-229E spike (S) genes and 5.7 × 10 -4 (95% HPD , 5-6.5 × 10 -4) s/s/y for HCoV-OC43 S genes, which were about fourfold lower than the 2.5 × 10 -3 (95% HPD , 2.3-2.7 × 10 -3) s/s/y rate for IAV hemagglutinin (HA) genes . Coronavirus S genes accumulated about threefold less (P <0.001) non-synonymous mutations (dN) over time than IAV HA genes . In both IAV and HCoV, the average rate of dN within the receptor binding domains (RBD) was about fivefold higher (P <0.0001) than in other glycoprotein gene regions . Similarly, most sites showing evidence for positive selection occurred within the RBD (HCoV-229E , 6/14 sites, P <0.05; HCoV-OC43 , 23/38 sites, P <0.01; IAV , 13/15 sites, P = 0.08). In sum, the evolutionary dynamics of HCoV and IAV showed several similarities, yet amino acid changes potentially representing antigenic drift occurred on a lower scale in endemic HCoV compared to IAV . It seems likely that pandemic SARS-CoV-2 evolution will bear similarities with IAV evolution including accumulation of adaptive changes in the RBD, requiring vaccines to be updated regularly, whereas higher SARS-CoV-2 evolutionary stability resembling endemic HCoV can be expected in the post-pandemic stage.