The Argentine was an unused substitute against Leicester in the club’s last Premier League outing, with Jesus on target in a 2-0 win over the Foxes.
Aguero did start a midweek Champions League clash with Feyenoord, though, and has retained his place for a meeting with Terriers.
Club captain Vincent Kompany also comes back into the starting XI, but there is no place in the matchday squad for Yaya Toure.
Man City team: Ederson, Walker, Otamendi, Kompany, Delph, Fernandinho, Silva, De Bruyne, Sane, Sterling, Aguero. Subs: Bravo, Danilo, Gundogan, Mangala, Bernardo, Jesus, Zinchenko.
Victory for City will see Pep Guardiola’s side restore an eight-point advantage at the top of the Premier League standings.
The Blues are yet to suffer defeat in any competition this season, with a free-scoring outfit sweeping aside all before them.
Huddersfield have slipped back into mid-table after making a bright start to life among the elite, but they have come unstuck on home soil just once so far.