In Man City transfer news, last season's Treble winners have agree a five-year contract with the 21-year-old, who scored 10 goals in 75 Ligue 1 appearances across three seasons.
Doku, who has 16 caps for Belgium, has taken the number 11 shirt.
"This is a great day for me, both personally and professionally. City are the best team in world football, so joining them is special," Doku said.
In other Man City transfer news, Doku becomes Pep Guardiola's third summer signing after midfielder Mateo Kovacic arrived for £25m from Chelsea and defender former RB Leipzig defender Josko Gvardiol joined for £77m.
West Ham, Tottenham and Chelsea had also been interested in signing Doku, who scored seven goals in 35 games last season.
Doku had two years left on the five-year deal he signed when Rennes paid 26m euros (£22.3m) to sign him from Anderlecht in October 2020, shortly after he made his international debut as a teenager.
Doku cited the opportunity to work under City boss Guardiola as a key factor in his decision to join the Premier League champions.
"I am a young player with so much learning and improving to do," added the Antwerp-born winger.
"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.
"Watching City last season was amazing. To win the Treble is the hardest thing in football and they did it. You cannot imagine how exciting it is to be joining this team. I cannot wait to get started. Hopefully I can make the fans happy", in Man City transfer news.
City's director of Football Txiki Begiristain has tipped Doku to develop into a "world class" attacking player under Guardiola's guidance.
He 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."