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The Quake 4 single player mode continues the story of Quake II by pitting the player against a cyborg alien race known as the Strogg. The game follows the story of a marine named Matthew Kane who is a member of the fabled Rhino Squad. Following the success of the protagonist of Quake II in destroying the Strogg's leader, the Makron, the Rhinos are tasked with spearheading the mission to finally secure the aliens' home planet Stroggos. In the course of the invasion, the squad ship is shot down and crashes in the middle of a battle zone, separating Kane from his companions. Kane eventually rejoins his scattered team members and partakes in the assault against the Strogg.

After performing a number of tasks, such as destroying and capturing Strogg aircraft hangars and defense systems, Kane and his remaining squad members make it to the USS Hannibal. There they are given their next mission: infiltrating one of the Strogg's central communication hubs, the Tetranode, with an electromagnetic pulse bomb in the hope that it will put the main Strogg Nexus in disarray. Kane is tasked with defending the mission convoy, which takes heavy casualties. After many setbacks, including the destruction of the EMP device by a Strogg ambush, Kane is left to complete the mission, assisted only by Private Johann Strauss and Lance Corporal Nikolai "Sledge" Slidjonovitch. Strauss figures out a way to destroy the core by shutting down its coolant systems. As Kane reaches the entrance to the Tetranode, however, he is greeted by two rocket-equipped network guardians - as well as the newly constructed Makron. The Makron easily defeats Kane and knocks him unconscious.

When Kane finally awakens, he finds himself strapped to a conveyor belt in the Strogg "Medical Facilities", a structure used for turning those captured and killed by the aliens either into protein food or additional Strogg units. In a long and gruesome first-person cutscene, Kane is taken through this stroggification process which violently replaces much of his anatomy with bio-mechanical parts. Before the final controlling neurochip implanted in his brain can be activated, though, Rhino Squad bursts into the facility and rescues Kane. After escaping through the Strogg medical facility and Waste Disposal plant, fighting off zombie-like half-stroggified humans along the way, Kane is forced to combat his former commander, Lieutenant Voss, who has been fully stroggified into a powerful mechanized monster. (Voss nevertheless retains his own consciousness long enough to warn Kane.) After defeating this threat, Kane and the remaining marines finally make it back to the Hannibal.

The commanders realize that Kane's Strogg physiology has opened up new possibilities for defeating the Strogg, as he can be used to infiltrate locations previously impenetrable to human forces. The new plan is to directly target the Strogg Nexus Core, a huge centralized brain-like structure which controls the alien forces. Rhino and Raven Squads are tasked with infiltrating the three data processing towers adjacent to the Nexus, a huge data storage and processing tower. There, they will deactivate the Nexus's shield and power up the teleporter used to access the Nexus and send Kane in. Once inside, Kane will travel to the center of the Nexus to destroy the Core Brain and its guardian.

After infiltrating the facility and realigning the data nodes powering the teleporter, and destroying its fearsome "Guardian" creature, Kane finally reaches the Nexus core. There he meets the Makron in a final showdown and kills it. This done, he destroys the Core and returns to the Hannibal. Celebrating with Rhino Squad afterward, Kane receives word that he has new orders.