The severe acute respiratory syndrome coronavirus (SARS-CoV) emerged in humans in 2002. Despite reports showing Chiroptera as the original animal reservoir of SARS-CoV, many argue that Carnivora-hosted viruses are the most likely origin. The emergence of the Middle East respiratory syndrome coronavirus (MERS-CoV) in 2012 also involves Chiroptera-hosted lineages. However, factors such as the lack of comprehensive phylogenies hamper our understanding of host shifts once MERS-CoV emerged in humans and Artiodactyla. Since 2019, the origin of SARS-CoV-2, causative agent of coronavirus disease 2019 (COVID-19), added to this episodic history of zoonotic transmission events. Here we introduce a phylogenetic analysis of 2006 unique and complete genomes of different lineages of Orthocoronavirinae. We used gene annotations to align orthologous sequences for total evidence analysis under the parsimony optimality criterion. Deltacoronavirus and Gammacoronavirus were set as outgroups to understand spillovers of Alphacoronavirus and Betacoronavirus among ten orders of animals. We corroborated that Chiroptera-hosted viruses are the sister group of SARS-CoV, SARS-CoV-2 and MERS-related viruses. Other zoonotic events were qualified and quantified to provide a comprehensive picture of the risk of coronavirus emergence among humans. Finally, we used a 250 SARS-CoV-2 genomes dataset to elucidate the phylogenetic relationship between SARS-CoV-2 and Chiroptera-hosted coronaviruses.