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Wounded by a gunshot from Russian assassin Kirill (in the previous film, The Bourne Supremacy), Jason Bourne evades Moscow police and goes into hiding.

Six weeks later, Bourne goes to Paris to inform Martin Kreutz of the death of his sister Marie, who had been Bourne's girlfriend. The Guardian correspondent Simon Ross meets with someone to discuss Bourne and Operation Treadstone. The CIA begin tracking Ross after he mentions "Operation Blackbriar" over a cell phone call. Bourne learns of Ross' investigation of Treadstone and they secretly meet at Waterloo Station. Bourne realizes that the CIA is tracking Ross and helps him evade capture, but Ross deviates from Bourne's instructions and is killed by Blackbriar assassin Paz, on orders from Blackbriar's director Noah Vosen.

Pamela Landy, who six weeks earlier had unsuccessfully hunted Bourne, is brought in to help Vosen. They search Ross' notes and find that Ross' source was Neal Daniels, now CIA Station Chief in Madrid, who was formerly involved in Treadstone and is actively involved in Blackbriar. Bourne also makes his way to Daniels' Madrid office, but finds it empty. After Bourne incapacitates a CIA team sent by Vosen and Landy, Nicky Parsons, a former Treadstone support technician now posted in Madrid, arrives. She decides to help Bourne and tells him that Daniels has fled to Tangier.

Upon arriving in Tangier, Parsons tries to track Daniels' location but is unable to, finding that Blackbriar "asset" Desh Bouksani has been tasked with killing Daniels. Vosen learns that Parsons logged in to access information about Daniels and sends Desh after Parsons and Bourne, a decision Landy disagrees with. Bourne follows Desh to Daniels, but fails to prevent Daniels' death by a planted bomb. Bourne manages to kill Desh before he can kill Parsons, and subsequently sends Parsons into hiding. Bourne examines the contents of Daniels' charred briefcase and finds the address of the deep cover CIA bureau in New York City where Vosen directs Blackbriar.

Bourne travels to New York City. Landy receives a phone call from Bourne (in a repetition of the final scene of The Bourne Supremacy), which is revealed to be tapped by Vosen. Landy thanks Bourne for the tape he sent her which revealed the corrupt dealings of former Treadstone director Ward Abbott; she also tells him that his real name is David Webb and his birthdate is "4-15-71". Bourne tells Landy to "get some rest" because she "looks tired", which she and Vosen both understand to mean that Bourne is watching her. Vosen intercepts a text to Landy from Bourne of a location to meet up and leaves his office with a team to follow Landy and capture Bourne. Bourne breaks into Vosen's office and steals classified Blackbriar documents. Vosen sends Paz after Bourne, the two finally encountering each other in a car chase which ends with Paz forcing Bourne's car into crash into a concrete divider. Bourne gets out and holds Paz at gunpoint before sparing his life and continuing on to 415 East 71st Street, memories of which were triggered by the false birthday he was given by Landy. Vosen also figures out Landy's code and warns Dr. Albert Hirsch, who ran Treadstone's behavior modification program, that Bourne is coming.

Landy meets Bourne at the building, where Bourne gives her the Blackbriar files before going inside. Landy starts faxing the files to an unknown receiver, but is found by Vosen as the last page is sent. Bourne encounters Hirsch in an upper level and, with Hirsch's help, remembers that he volunteered for Treadstone. He then states that he is no longer Jason Bourne and flees to the roof from Vosen's pursuing CIA team. Bourne is confronted on the roof by Paz, who asks Bourne why he did not kill him. Bourne asks Paz if he even knows why he is supposed to kill him and repeats the dying words of a Treadstone assassin Bourne killed years earlier (in The Bourne Identity): "Look at us. Look at what they make you give." Paz lowers his gun as Bourne runs to jump off the roof, but Vosen appears and shoots at Bourne as he leaps into the East River below. Some time later, Parsons watches a television news broadcast about the exposure of Operation Blackbriar, the arrests of Hirsch and Vosen, a criminal investigation of CIA director Ezra Kramer, and David Webb, a.k.a. Jason Bourne, who was reportedly shot and fell into the East River. Upon hearing that his body has not been found after a three-day search, Parsons smiles. Bourne is shown swimming away under water after his fall.

In the Mediterranean Sea near Marseille, Italian fishermen find an unconscious man floating adrift with two gunshot wounds in his back. The boat's medic finds a tiny laser projector surgically implanted under the unknown man's skin at the level of the hip. When activated, the laser projector displays the number of a safe deposit box in Zürich. The man wakes up and discovers he is suffering from amnesia. Over the next few days on the ship, the man finds he is fluent in several languages and has unusual skills, but cannot remember anything about himself or why he was in the ocean. When the ship docks, he sets off to investigate the safe deposit box.

At CIA headquarters in Langley, Virginia, Deputy Director Ward Abbot learns about a failed assassination attempt against exiled African dictator Nykwana Wombosi. Meanwhile, in Zürich, the amnesiac incapacitates two police officers using advanced hand-to-hand combat when they attempt to arrest him. The next morning, he visits a bank using the number that was embedded in his hip, and opens a safe deposit box to find several passports containing his picture (all under different names and nationalities), large amounts of assorted currencies, and a handgun. He assumes the name from the first passport, Jason Bourne. He takes all the passports and money, but leaves the handgun.

As he leaves, a bank employee contacts Operation Treadstone, a CIA black ops group. After being chased by police, Bourne escapes into a U.S. consulate where he is again pursued by authorities. Bourne escapes and encounters a Swiss woman named Marie Kreutz, offering her $20,000 to drive him to an address in Paris. Meanwhile, Alexander Conklin, the head of Treadstone, assures Abbott that he will destroy any evidence connecting them to Bourne, who was responsible for the failed assassination attempt on Wombosi. He activates three "assets" to take down Bourne: Castel, Manheim, and The Professor.

Bourne arrives at the address on his passport, and after studying the apartment, hits redial on his phone and is connected to the Hotel Regina, which recognizes Bourne's alias from a British passport. Bourne is told that Kane died two weeks before in a car crash. Castel ambushes Bourne and Marie at the apartment, but Bourne manages to defeat him after a fight and attempts to interrogate him unsuccessfully. Marie finds wanted posters in Castel's bag with both her and Bourne's pictures on them; as Bourne attempts to calm her down, Castel jumps out of a window to his death. Marie goes into shock, and Bourne escorts her from the building.

Conklin plants a body in a Paris morgue in an attempt to fool Wombosi into thinking Kane is dead, but Wombosi recognizes that the body is not his assailant. The Professor assassinates Wombosi at his home. Bourne investigates Wombosi and concludes that he was an assassin prior to his amnesia. He and Marie leave the city and travel into the French countryside to stay at the house of Marie's stepbrother Eamon, where Bourne decides that he no longer wants to be who he was. In the morning, The Professor comes to kill Bourne. Bourne uses a shotgun to blow up a propane tank and cloud the view of the sniping Professor. After a brief standoff in a cropfield, Bourne shoots The Professor twice and interrogates him briefly. The Professor reveals their mutual connection to Treadstone before dying. Bourne sends Marie away for her own safety. He contacts Conklin to arrange a meet, but instead tracks Conklin's vehicle to discover the location of Treadstone's safe house in Paris.

Bourne breaks in and holds Conklin and logistics technician Nicky Parsons at gunpoint, beginning to remember his last mission through successiveflashbacks. "Kane" was an assumed identity during his mission to infiltrate Wombosi's entourage and kill him, but Bourne failed to kill Wombosi aboard his yacht when he intended to because his children were sleeping nearby. Bourne fled and was shot twice in the back in the process. Bourne tells Conklin that he is leaving Treadstone and warns not to follow him. Realizing that their conversation is being overheard, Bourne leaves Conklin and Parsons before killing two agents who try to kill him. Abbott shuts down Treadstone and has Manheim kill Conklin. Abbott goes before an oversight committee, dismissing Treadstone and previewing a new project codenamed "Blackbriar". Some time later, Jason finds Marie renting out scooters to tourists in Greece, and the two reunite.

Following where the previous film left off, Alice (Milla Jovovich) and the others on the Umbrella Corporationfreighter Arcadia face an attack by a fleet of airships led by Alice's former ally Jill Valentine (Sienna Guillory), who has been brainwashed by Umbrella through a red scarab device attached to her chest. When Alice causes an airship to crash into the ship, she is knocked unconscious into the water.

Switching over into what seems to be an alternate reality, Alice finds herself living as a suburban housewife with her husband Todd (Oded Fehr) — a clone of Carlos Olivera — and deaf daughter Becky (Aryana Engineer). However, this idyllic life is disrupted when zombies attack and kill Todd. Alice and Becky escape to the streets and are rescued by Rain Ocampo (Michelle Rodriguez), who lets them ride in her car. As the three escape, they are hit by a truck, knocking Rain unconscious while Alice and Becky escape. Alice runs and is attacked by a zombified Todd.

The scene ends when the real Alice awakens in an Umbrella base, having been captured at the Arcadia. Jill interrogates Alice, who unsuccessfully pleads with her to remember her true identity. During an unexpected power failure, Alice escapes from her cell. After battling a horde of zombies, Alice encountersAda Wong (Li Bingbing), an associate of Albert Wesker (Shawn Roberts). Ada explains that she and Wesker no longer work for Umbrella. Wesker appears and, seeming to have redeemed himself, reveals that the Red Queen is now controlling what's left of Umbrella and he plans to aid Alice's escape and battle the base's programs, in order to save what's left of mankind. Ada also reveals that the base is underwater and serves as a testing ground for experiments. Additionally, Wesker has organized a team of freelance operatives to infiltrate the base and help Alice and Ada escape, including Leon S. Kennedy (Johann Urb),Barry Burton (Kevin Durand), and Luther West (Boris Kodjoe).

Leon's team plants explosives near the entrance of the base, which will detonate in two hours and trap anybody still inside. The group plans to meet with Alice and Ada in a simulated Raccoon City suburbia, identical to the one in Alice's flashback. As Alice and Ada walk through a simulation of New York City, they defeat two Axemen. Leon and his team enter a Moscow simulation, but are cut off by armed Las Plagas zombies. Alice and Ada manage to enter the suburban simulation where they were supposed to meet up with Leon and his team. In the arena the two find Becky, as well as Jill and her mercenaries, consisting of clones of Alice's deceased allies: Rain, Carlos and James "One" Shade (Colin Salmon). A shoot-out occurs, resulting in Ada being captured and Alice and Becky escaping.

Alice and Becky run into the "good" Rain and head to Moscow, where they meet up with Leon's team. The group escapes the intelligent zombies, and reach an elevator that leads them to submarines that could help them escape, although it shuts off. An enormous licker appears, with it capturing Becky and killing "good" Rain. The group pursues the licker, where they encounter Jill's group; another battle ensues, in which Barry is killed but not before he kills One. Alice manages to rescue Becky. During their escape from the licker they arrive at a cloning facility where Alice and Becky see multiple copies of themselves. Realizing this Becky pleads and asks Alice to tell her the truth, at which Alice declares that she is now her mother. Then she goes to the pod where she rescued Becky from, killing the licker and destroying the cloning facility. They rejoin Leon and Luther as the detonation occurs. The explosion results in the flooding of the facility and the death of Carlos.

The group reaches the surface; however, they are met by a submarine, from which Jill, the evil Rain, and a captured Ada emerge. With new orders from the Red Queen to kill Alice, Jill battles Alice while Rain, injecting herself with the Las Plagas parasite that gives her strength and apparent invincibility, knocks out Ada and fights Leon and Luther, with Luther being killed in the process. Alice manages to remove and destroy the scarab device from Jill, returning her to normal. Alice joins Leon in fighting Rain; she notices there are zombies from the facility swimming up to the ice. She shoots the ice where Rain is standing, and she falls in the water, leaving her fate to the zombies. Alice, Ada, Becky, Leon, and Jill (who is no longer being controlled by the Red Queen) travel to Wesker's base: the heavily barricaded and guarded White House. Wesker injects Alice with the T-virus, returning her former superhuman powers in order to enact his plan, then tells her that she is responsible for saving the remaining humans from extinction once and for all. Wesker then leads them up top of The White House, explaining that this is the last stand of the human race. The scene zooms out to reveal the landscape around them, showing destroyed Umbrella helicopters, volcanic craters and the remaining U.S troops and Wesker's Umbrella army fighting against enormous hordes of zombies and mutant creatures.