Doku has effectively been signed as a replacement for Riyad Mahrez, who joined Saudi Arabian side Al Ahli earlier this month.
Doku has penned a five-year contract at the Etihad Stadium.
In three seasons in Ligue 1, the 21-year-old recorded 10 goals in 75 appearances for Rennes.
Doku is of Ghanaian descent but has been capped 14 times by the Belgium national team, including one appearance at the 2022 FIFA World Cup in Qatar.
"Manchester City are the best team in world football, so to be joining them is something very special for me and my family," Doku told the Man City website.
"I am a young player with so much learning and improving to do. Working with Pep and his staff, and playing alongside these world-class players, will make me a much better player. I feel sure of that."
City's director of Football Txiki Begiristain added: "Jeremy is a very exciting young player and I'm so pleased he's joining us.
"In terms of raw attributes, he has everything a winger needs. He has outstanding pace and he is exceptional in one-on-one situations.
"I honestly believe working with Pep and the technical staff here at City will see him develop into a world-class attacking talent."
Doku is Manchester City's third summer signing after Josko Gvardiol and Mateo Kovacic.