Until 2017, Huntington was generally controlled by the Democratic Party, having the same Democratic town supervisor, Frank Petrone, for 20 years prior to 2017. The town board followed suit during these years, generally being controlled by the Democratic Party. In 2017, the Republican Party took control of the town supervisor position with the election of Chad Lupinacci. The Republicans have held this position since. In the 2021 general election, the people of Huntington elected Edmund Smyth to the supervisor position. Two Republicans were also elected to the town board: Dr. Dave Bennardo and Salvatore Ferro. In the 2023 general election, Brooke Lupinacci and Theresa Mari were elected, creating a 5–0 super majority for the Republican Party on the town board. The town clerk position is held by Andrew Raia, and the highway superintendent is Andre Sorentino, both Republicans. The lone Democrat in the Huntington town government is Jillian Guthman, who has served as the receiver of taxes since 2017, when she was appointed to the position by the board, and shortly after re-elected to serve a full term in 2018.