The game picks up where Escape from Butcher Bay left off. Following Riddick and Johns' escape from the Butcher Bay Correctional Facility, both men are deep in cryogenic sleep. Riddick wakes up early and is witness to their escape ship being dragged unwillingly into the Dark Athena, a gigantic mercenary vessel run by Gale Revas and her second in command, Spinner. Riddick avoids capture as Revas and her men take Johns away. Using the same stealth tactics as he did in Butcher Bay, Riddick sneaks and hides throughout the ship seeking to escape, killing the guards and mercenaries he encounters along the way. Many of the guards are automated drones, human bodies with implanted machine parts and a primitive AI, that can be controlled remotely from within the ship.
There he meets with a little girl named Lynn who is also hiding from the guards. Riddick makes his way to the prison cells and finds several people captured, including the former Captain of the Dark Athena, Irvin Senate. There he meets Lynn's mother, Ellen Silverman. She offers to make Riddick the tools he needs to escape through the air vents if he can get the right parts. She also asks to find Lynn because she is concerned for her safety.
In order to find the parts she needs Riddick must help yet another prisoner, Jaylor, have his revenge against the man who put him in the cell, Margo Marvins. On his way to kill Margo, Riddick comes across the massive Ironlord and kills him in one on one combat.
During this time, a prisoner named Max Dacher offers his technical skills to help Riddick escape on a ship and unlock doors for him if Riddick can find him a data pad. He agrees and finds the data pad for Dacher and the parts for Silverman. After again meeting with Lynn, Silverman keeps her word and makes him the tool he needs. Riddick moves on and is in contact with Dacher via video communication at computer terminals on the ship. Riddick frees the prisoners inciting massive ship wide riots. During this time Riddick controls a drone. Riddick meets back up with Silverman, but she is killed by Jaylor. After disposing of Jaylor, Riddick makes his way to the escape ship.
On-board the escape vessel, Revas surprises and kills Dacher as he prepares the ship. Riddick finally meets Revas face to face and a battle ensues. As they fight, he wounds her severely and she appears to be dead. Finding the ship to not be working Riddick prepares and enters an escape pod. Just before he is to take off, Lynn shows up and starts pounding on the door begging to take her with him. Revas, who is still alive as Riddick's pod takes off, fires a missile that hits the pod, causing it to crash on the planet Aguerra Prime below.
Riddick wakes up on the shore of a beach (the same beach seen in the introductory tutorial level) and he makes his way into an abandoned city. The planet is under siege from Revas' troops who are killing all the civilians and harvesting their bodies to use for their drones. Riddick realizes his only way off the planet is to get back on the Dark Athena again. He makes his way through the city and back to the port where the Athena is docked. Spinner attacks Riddick in a robotic mech suit but is defeated. He gets back onto the Dark Athena and meets Lynn again. She tells Riddick her mother taught her how to make the drones turn on Revas' crew and attack them instead. Fighting ensues on the ship between the drones and the mercenaries. He makes his way up the ship and Riddick meets with Revas again, who now wears a suit of armor with heavy weapons. He defeats her by pushing her into an elevator shaft and she falls to her death. Lynn meets up with him and they are seen going into the elevator. She asks him if Revas is coming back, and Riddick answers "When I say goodbye, it's forever." Then the credits roll.