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Boston has a surviving militarized quarantine zone. A portion of the city sits behind a high wall that is frequently patrolled for infected and stragglers alike. Its citizens live under a police state drafted into service. Food is rationed and people sometimes turn to eating rats. The Boston QZ has a thriving underground, drug and gun trade as well as a sizable group of Fireflies. When Marlene is injured, she turns to resident smugglers Joel and Tess to smuggle Ellie out of the zone, and to the Capitol building downtown. Much of the downtown area shows the damage done by the bombings outside the QZ not long after the outbreak began. Nature is beginning to reclaim the empty parts of the city, underground basements are flooded, and neglected structures are crumbling away. The abandoned parts of the city and outlying areas are infested with Clickers, Runners. There is also a black market area, housing the smugglers.
Joel and Ellie come to Lincoln to look for Bill, whom Joel claimed to have a working car which they could use to go west and bring Ellie to the Fireflies. Lincoln is home to Bill, Frank, and hordes of infected. The city of Lincoln is full of traps, which keep the infected at bay. Bill, Joel, and Ellie fight their way through Lincoln to reach a crashed military vehicle, which had some parts that Bill needed to fix a car for them. Lincoln is also the place where the Bloater is first encountered.
On their journey west, Joel and Ellie become stuck in the city of Pittsburgh, which is home to the Hunters, hostile survivors who survive by killing and robbing others. They refer to their potential victims as "tourists". Joel and Ellie are pursued by the Hunters and their armored vehicle, which is equipped with a .50-caliber machine gun. As they fight their way through Pittsburgh, Joel and Ellie meet two more survivors, Henry and Sam. With a common destination (the Fireflies), they decide to stay together and fight their way to a radio tower where Henry is expecting to meet other survivors. On their way to the tower, Sam is bitten and starts to turn overnight. In the morning he attacks Ellie and is shot by Henry. Henry then kills himself out of grief.
As they make their way westward, Joel and Ellie stumble across a hydroelectric dam, which is being used to power a small town. This town is home to Tommy and Maria. The dam is attacked by raiders, who are defeated by Joel and Tommy. Ellie steals one of Tommy's horses and hides in an abandoned house, and Joel and Tommy promptly pursue her, combating numerous raiders along the way. Joel wants Tommy to take Ellie to the Fireflies, but she expresses that she wants to stay with Joel. Tommy reveals to Joel that the Fireflies have a camp at the University of Eastern Colorado, so Joel takes Tommy's horse to continue their journey.
At the end of the game, Joel and Ellie return to Jackson County, presumably to live there with Tommy.
Upon arriving at the UEC, Joel and Ellie must reach the science building, which is where the Fireflies are supposed to have located their medical research and personnel. Joel battles the numerous infected that inhabit the abandoned UEC, only to find that the Fireflies have relocated to Salt Lake City. On their way out they are attacked by bandits from David's group of cannibals, and Joel is grievously wounded after he falls on a piece of rebar following a struggle with one of the attackers (who is killed in the fall).
Ellie takes Joel to recuperate after he is wounded to the Lakeside Resort, which also happens to be the headquarters of David's group of cannibals. As she pursues a deer, she meets David, and bargains with him to trade the deer meat for some antibiotics. David and Ellie fight off waves of infected that followed her during her pursuit of the deer, and after David's partner returns with some penicillin he sends some of his cannibals after her. Tommy's horse is shot during her escape, and Ellie is trapped in the town where the cannibals reside as a blizzard hits the resort. During this time, Joel awakens to find Ellie missing, and he follows her into the resort. Ellie kills David after a brutal fight, and Joel takes her to Salt Lake City.
After finally reaching Salt Lake City, Joel and Ellie see a herd of giraffes that have escaped from the zoo, and are peacefully eating the foliage that has grown on the buildings. They encounter numerous infected, including three Bloaters, while trying to get through the underground highway. Ellie almost drowns, and while attempting to resuscitate her, Joel sees a group of Fireflies approaching. They are taken to St. Mary's Hospital, and Ellie is drugged to prepare for the surgery. Marlene reveals to Joel that the surgery will end Ellie's life, so Joel battles the Fireflies to rescue her.