"Following a trophy-laden 12 years at the Etihad Stadium, Txiki will leave his current post following the club's involvement in this summer's FIFA Club World Cup and will be succeeded by Hugo Viana of Sporting CP," the club said.
"Viana will begin his full-time role in the summer of 2025, but will collaborate with Txiki in the preceding months to ensure a smooth transition.
"We look forward to paying tribute to Txiki's outstanding contribution to Manchester City at the end of the season."
Begiristain joined City in 2012 after working in the same role at Barcelona between 2003 and 2010.
The Spaniard was widely credited with convincing his former Barcelona team-mate Guardiola to become City manager in 2016.
Begiristain had given Guardiola his first managerial job at Barcelona, with the pair striking up a close friendship when they played for the Spanish club in the 1990s.
City have enjoyed a golden era with Guardiola and Begiristain calling the shots.
They have won six Premier League titles, including the last four in a row, and the club's first Champions League crown among a host of other trophies.
Begiristain's impending exit will raise further questions about Guardiola's future with his contract expiring at the end of this season.
The 53-year-old has yet to agree an extension after hinting last season that he could be near the end of his time in England.