The single-player part only serves as a diversion for the online multiplayer options, with modes such as duel, team deathmatch (TDM), capture the flag (CTF), and more. Not everything was kept - the double-jumping from the previous titles was removed for instance, but replaced with new tricks.

The game offers more speed than Quake 2, but it is not as fast as the original Quake. Advanced players use techniques such as rocket jumping, strafing, and circle jumping to quickly get around areas. As with the other Quake games, it is known for its freedom in movement. The different arenas are also filled with health bubbles, complete sets of armour and armour shards, the well-known Quad Damage power-up, ammunition, and specials such as Mega Health, Haste, Invisibility, a powerful Battlesuit, and more.

Each weapon has specific advantages, ranging from the amount of damage to reloading times and the ability to hit-scan opponents. The player's arsenal consists of new and familiar, but redesigned weapons, including a gauntlet (melee attacks) and a machine gun as the spawn weapons, a shotgun, plasma gun, lightning gun, rocket launcher, railgun, and BFG. Compared to the previous titles, the colours and general design of the game are much brighter and it shakes off the dominant shades of brown and grey the previous titles in the series were known for. The offline part takes the player through a number of one-on-one and team-based challenges against AI-controlled opponents, slowly ranking upwards in difficulty, as the character of the player's choosing. The third game in the Quake series is a departure from the previous games, focusing exclusively on multiplayer arena fighting with no story-driven singleplayer part - directly competing with Epic Games that did the same with the contemporary Unreal Tournament.

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