The Manchester United forward was caught on camera goading the home supporters after the derby.
Zirkzee could not resist having the last laugh as he approached the fans behind the United dugout at the Etihad Stadium.
It followed the Red Devils' dramatic late turnaround over their bitter rivals.
Goals from Bruno Fernandes and Amad Diallo two minutes apart secured a 2-1 win for Ruben Amorim's side.
Second half substitute Zirkzee played the final 12 minutes off the bench.
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He impressed in his cameo after replacing Rasmus Hojlund in attack.
Following the final whistle, the Dutch striker returned to the dugout to celebrate the victory.
Footage from the stands shows Zirkzee approaching the fans behind the technical area as he pumped his fists and cheers.
Several home fans can be seen responding by swearing at the United star.
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Reacting to the incident on social media, one Red Devils fan wrote: "What s***housery, love that."
Another added: "That's my goat."
A third supporter also commented: "He was so hyped up. I love it."
Sunday's win has boosted United's slim top four hopes as they snatched a first win at the Etihad since March 2021.
Despite remaining 13th in the table, the Red Devils are only six points adrift of fourth place Nottingham Forest.
They have also cut the gap to City in fifth down to five points with 16 matches played.
United will hope to take their momentum into Carabao Cup action this week.
Amorim's side visit Tottenham in the quarter-finals on Thursday night.
Dwight Yorke gives warning to Manchester Utd fans about Joshua Zirkzee and Rasmus Hojlund