The 2023 world champion started sixth on the grid but after eventually passing leader Lando Norris halfway through the race, Verstappen held off a late challenge from 2021 nemesis Lewis Hamilton to claim his 50th Formula 1 win.
Later, Hamilton and Charles Leclerc were disqualified from the race.
Yet as Verstappen walked out onto the top step of the podium, the Dutchman was booed by sections of the fanbase in Austin.
There were also chants from spectators – who by this point had made their way onto the main straight as is custom post-race – during the Dutch national anthem which followed.
Verstappen has faced jeering before, most notably at Silverstone last year, and was clearly not a fan favourite at the Circuit of the Americas, especially compared to the likes of Hamilton and Norris.
Verstappen claimed his 15th win of the season but unlike many Sunday cruises this year, he was made to work.
The Red Bull driver was also complaining of brake issues throughout the 56-lap race and not for the first time this year, he was involved in numerous frosty exchanges with his race engineer Gianpiero Lambiase.
Lambiase came onto the team radio while Verstappen, at times, was braking in corners - with the Dutchman unimpressed by the interventions.
Verstappen admitted after the race that Hamilton’s Mercedes team “could have won today if they’d done a better strategy” but was nonetheless satisfied with the victory.
Austin was the first in a triple-header, with the paddock heading on to Mexico City next week.