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* [[James Brolin]] as the narrator who is later revealed as the older Gus by the end of the final season<ref>{{cite web|url=https://www.cbr.com/sweet-tooth-james-brolin-interview/|title=Sweet Tooth: James Brolin Ponders Bringing the Narrator On-Screen|website=[[Comic Book Resources|CBR]]|first=Katie|last=Doll|date=May 4, 2023|access-date=June 6, 2024|archive-date=July 11, 2023|archive-url=https://web.archive.org/web/20230711004209/https://www.cbr.com/sweet-tooth-james-brolin-interview/|url-status=live}}</ref>
* [[Will Forte]] as Pubba (seasons 1 and 3),<ref name="AddMainNames"/> Gus's father<ref name="Maincastnames"/> who raised him in a secluded cabin in [[Yellowstone National Park]] to protect him from the outside world of hatred towards hybrids. It is later revealed that his name is Richard Fox and was a janitor at Fort Smith Labs in Goss Grove, Colorado.
* Naledi Murray as Wendy (seasons 2–3
* [[Neil Sandilands]] as General Abbot (season 2;<ref name="S2Maincast"/> recurring season 1), the leader of the Last Men who hunts hybrids. It is later revealed that his first name is Douglas.
* [[Marlon Williams (musician)|Marlon Williams]] as Johnny Abbot (season 2;<ref name="S2Maincast"/> co-starring season 1), General Abbot's younger brother
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