The Conduit is a first-person shooter, taking place in the near-future, as Washington D.C. is under the invasion of an alien race known as the Drudge. These aliens make use of portals, called Conduits, to deploy their forces through-out the city.

The player takes on the role of Secret Service agent Michael Ford, newly inducted into the shadow government organization of Trust after saving U.S. President Charles Thompson during an assassination attempt. Sent initially to disrupt a terrorist attack and recover stolen Trust technology, Fords finds himself soon betrayed by his employers and fighting against the hordes of invading Drudge.

A unique feature in the game is the Trust prototype recovered at the beginning of the game, known as the All-Seeing Eye, which can be used to detect hidden objects and enemies, a key feature in solving the game's puzzles.

Multiplayer includes 13 multiplayer modes for online play, which include the classic deathmatch and capture the flag modes, but also others such as the "ASE Football", where the player who captures the All-Seeing Eye, and holds it the longer wins.