At the dawn of the City Age, Tallulah was a prominent Hunter. She frequently brought other Hunters together for missions, including a rescue effort in Old Russia and working with Tav and Venra on supply recovery operations.
After the destruction of the Iron Lords, the Last City was engulfed in turmoil. The Speaker rose to power and tried to install a sense of order by helping form the Vanguard alongside the Titan Saint-14 and the Warlock Osiris. Tallulah was approached by the Speaker and was asked to join as the Hunter's representative and leader at the suggestion of Saint-14. She was unamused by the idea, informing the Speaker that organizing Hunters made little sense, as they tended to be independent and have little time or patience for rules and regulations. The Speaker noted that she had already been organizing and bringing Hunters together on other missions, but she took offense to him describing them as solitary and countered they were independent instead. However, when the Speaker mentioned that although she was the preferred choice there were other candidates to be selected as Hunter Vanguard, Tallulah's competitive nature emerged. She stated that it would be difficult to make time for logistical issues, and the Speaker agreed it would be a daring challenge for someone with her schedule. With a dare now being offered, Tallulah took the Speaker's offer much more seriously and agreed to become the Hunter Vanguard.
Eventually the Faction Wars broke out into opening fighting as various Ghostless and Guardian-led factions fought for power and influence in the Last City. Tallulah met with the Speaker, Saint-14, and Osiris to determine what the Vanguard's response would be. She noted that the City had been built to unite humanity but that it was now all breaking down from the inside. As the Speaker and Osiris argued over what role the Traveler was playing in the violence by creating Risen in the first place, Tallulah interrupted and stated that this was not about the Traveler, but a lack of real leadership, nervously worrying that all they had done was pack potential Warlords into one confined space with citizens surrounding them. Saint-14 suggested that a governing body with a representative from each faction should be formed, although the Speaker declared that too many factions had dangerous ideas or were violent. Despite Osiris' objection to how dangerous ideas would be defined, Tallulah supported the proposal and began listing factions she believed were violent and had to be exiled, including Echelon South and the Binary Star Cult, while also reporting rumors that a recently formed faction, New Monarchy, was also behind some of the violence. Following the conclusion of this meeting, hearings were held to judge the factions, and three of the most prominent remaining ones were selected to join the newly formed Consensus alongside Tallulah and the other Vanguard leaders.
At some point in her career as the Hunter Vanguard, Tallulah was playing cards against a kind-looking old grandfather. Dealing their hands was an Exo and apparent friend of the Hunter Vanguard's, Caliban-8. The game started well for Tallulah, and she excitedly envisioned herself telling the story of her winnings back at The Tower. However, at some point during the game, both Tallulah and Caliban took notice of the true nature of the other player sitting at the table and discovered that it was actually an Ahamkara, a shapeshifting, wish-granting creature, disguising itself in human form. After this discovery, the Hunter Vanguard continued to play against the Ahamkara, eventually coming down to a bet for her life. It is believed to be here that she also gave Caliban-8 the Vanguard Dare, saying that if she lost her hand (and subsequently, her life), he would succeed her position as Hunter Vanguard.
Caliban called Tallulah's bet, and immediately begged and pleaded desperately with the Hunter Vanguard to take it all back, not to leave him. However, before the cards were down on the table, the three members of that game knew who won the bet. Upon losing, the Hunter Vanguard tossed her bow to the exo. As the Ahamkara came around the table to collect its winnings, Tallulah looked at her friend, who was speechless in horror, and simply said "A Dare's a dare, man. Good luck."
She was then killed by the Ahamkara; according to Caliban-8, she did not scream.
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