In the wake of pandemics like COVID-19, which have zoonotic origins, the role of wildlife as reservoirs for emerging infectious diseases has garnered heightened attention. Migratory birds, traversing continents, represent a potent but under-researched vector for the spread of infectious diseases, including novel coronaviruses. This study delves into the genetic diversity and transmission dynamics of coronaviruses in migratory birds, presenting pivotal findings. From April 2019 to April 2023, we screened 5,263 migratory bird samples collected from Shanghai, China, identifying 372 coronavirus-positive samples belonging to five avian-related coronavirus subgenera and subsequently obtaining 120 complete genome sequences. To facilitate further research with a global perspective, the study curated all available 19,000 avian-associated CoVs and expanded the original 12 species to 16, including three novel coronavirus species identified in our study and one re-classified species from the public domain. The study illuminates the intricate genetic evolution and transmission dynamics of birds-related coronaviruses on a global scale. A notable aspect of our research is the identification of complex recombination patterns within the spike protein across different virus species and subgenera, highlighting migratory birds as a reservoir of coronavirus. Notably, the coronaviruses found in migratory birds, predominantly from the orders Anseriformes, Charadriiformes, and Pelecaniformes, with domestic ducks from Anseriformes playing a key role in bridging the transmission of coronaviruses between migratory and non-migratory birds. These findings reveal the genetic and recombination characteristics of coronaviruses in migratory birds, emphasizing the critical role of ecologically pivotal bird species in coronavirus transmission and genetic diversity shaping.