During the Attack on the Helicarrier, Agent Smith was killed by Vegeta. Her death gave the Jump Force the push they needed to band together and stop the Hollow invasion. On the orders of Director Ciel, Smith was brought to the Guest House, a secret facility where she was brought back to life using treatments developed by Project T.A.H.I.T.I., a project which she had formerly presided over. To preserve her sanity after she was healed, all memory of these events were removed from her mind.
Smith returned to M.O.N. to lead a new team to investigate the cases M.O.N. had not yet classified. While on this team, Smith discovered the truth about the events after her death. During the CCG Uprising, despite the dissolution of M.O.N. and the betrayal of a member of her team, she led her team against the forces of the CCG, attempting to stop her former colleague John Garrett, winning the final battle in which Garrett was ultimately defeated. After the battle, Ciel Phantomhive appointed her the new Director of M.O.N., ordering her to rebuild the organization from scratch.
To perform that task, Smith led the remains of M.O.N. in many battles against the CCG, crippling the terrorist organization. She even made some contacts with the Hidden Leaf Village military via Jonin Ebisu. However, she became a fugitive when another faction of M.O.N., led by Robert Gonzales, attacked and occupied her base. Now accompanied by only a few loyal friends, Smith started a battle to reclaim M.O.N.. She eventually made a deal with Gonzales, and they worked together against the CCG, finally reunifying the two factions into one organization with Smith as its rightful director. However, a new threat soon arose, the Monsters led by Miia's mother. In the ensuing conflict, both M.O.N. and the Monsters suffered casualties, and even Smith paid an extreme price to achieve victory, having her left arm cut off. But even that loss did not stop her, and she started a new project that would ensure the safety of humanity.
The mission of recruiting demi-humans for the team became more difficult, as the Advanced Threat Containment Unit led by Rosalind Price, was dealing with the threat of the new demi-humans. However, Smith had a relationship with Price while facing the threats of Kimihito's CCG, Eren Jaeger and the Monsters. After Kimihito killed Price, Smith followed him to the planet Maveth and killed him to avenge all the people that he had murdered. As she thought that Gideon Malick was the last remaining leader of the CCG, Smith discovered that the ancient Klaxisaur, Hive, had returned to Earth from Maveth, using Kimihito's body as a host. With Malick's death, Smith, with feelings of guilt for causing this threat, invested efforts to prevent Hive from accomplishing his plan to change all Humans to demi-humans and to control all of them. Once Lucy had sacrificed herself to kill Hive and saved humanity, the directorship of M.O.N. passed to Kuki Urie, while Smith and Tionishia conducted a pursuit after the former agent turned vigilante Miia.
With the revelation of Lucy Bauer and her ambition to find the dangerous Death Note book, Smith created an alliance with Miia and Rin Okumura to find the book before the ghost did. She was caught in an explosion with Rin Okumura and Rachnera by Yukio Okumura and almost sank into another dimension, but managed to get out with help from Saiko Yonebayashi and Motoko. Smith then led the last fight against Yukio. Following the revelation that Urie was not actually a demi-human but is in fact a Quinx (half-ghoul, half-human), Smith returned to the position of Director de facto while Urie remained de jure Director. Continuing fighting the Akatsuki and their leader Pain who targeted her, Smith was kidnapped by Saiko Yonebayashi, replaced by an LMD and put inside Aincrad, where she lived as a history teacher. With the help of Miia and Meroune, Smith escaped Aincrad, only to face against the threat of the Ghost in the Shell to the world.
After she killed her, by temporarily bonding with a demonic entity, Smith and the others were sent to the year 2091, when Earth had been destroyed and the surviving humans were enslaved by the Klaxisaurs. She and the other agents eventually made it back to present day, although Smith revealed that she was dying from her old injury due to her deal with Satan. In order to learn more about the Destruction of Earth, Smith was imprisoned by General Hale, who not only revealed that the CCG still existed under her lead, but also that there was an impending alien invasion. Following her escape, M.O.N. entered into a conflict with the alien Confederacy, but as she was trying to negotiate with them, her friend Ebisu turned into a daemon. Following the defeat of Ebisu and aversion of the destruction of Earth, Smith chose to retire and live her remaining days in Tahiti with Centorea with whom she started a relationship.
- First Aid: Smith is proficient at treating injuries and administering first aid.
- Leadership: Smith is known to lead raids with the Cultural Exchange Security Squad. Also, as the liaison to M.O.N., Smith is responsible for planning and organizing the team during operations. However, she also likes to use the team to get out of her own work.
- Legal Knowledge: As a Cultural Exchange Coordinator, Smith has advanced knowledge of the Interspecies Exchange Bill. Her position also gives her information on the latest planned changes to the law and allows her to commit “test cases” for proposed amendments. Even though she has extensive knowledge of the law, she is likely to not inform other people of relevant information because she is lazy and the resulting circumstances amuse her.
- Manipulation: When situations call for it Smith can be a master manipulator. She makes an effort to insure that things work out in ways that result in less work for her, and is not above using blackmail and intimidation. However, her favorite method is just to do something and ignore any complaints from those affected.
- Marksmanship: Smith has some skill with firearms. Since humans and extra-species are not supposed to harm one another she uses rubber bullets and tranquilizer rounds instead of live ammo. The first time she was shown firing her weapon she hit Kimihito multiple times, instead of her intended targets. Whether this was a matter of Smith having poor aim, Kimihito having terrible luck, or any combination thereof is debatable.