For unknown reasons, Venat objects to the Occurian method of controlling history by giving power to Man as a means to manipulate them. It questions the right of Gerun, leader of the Occuria, to dictate the destiny of Ivalice when by their nature the Occuria are exempt from time and do not live among the mortals.
Venat's truest desire is for the races of Ivalice to be freed from the grip of the Occuria, and it seeks to accomplish this by giving nethicite to the Archadians so they may overthrow the descents of Raithwall, the Dynast-King the Occuria would put in power. Though the Archadians are a means to an end, Venat does not control them as the Occuria control others - it considers Cid and Vayne Solidor friends and is considered the same in return.
Six years before the start of Final Fantasy XII, Dr. Cid traveled to the Jagd Difohr and found the Ancient City of Giruvegan, the place where mortals can access the Great Crystal, home of the Occuria. He met Venat who took Cid as its pupil. Returning to Draklor Laboratory, Venat guided Cid to create manufacted nethicite, granting the Archadian Empire vast new power they began to use to conquer Ivalice. Venat often accompanied Cid, but was invisible to others and could not be heard by them, making it appear Cid was speaking to himself, and thus it was feared he was going mad.
The first two times the party encounters Venat, they do not know what it is they see. Venat possesses Fran's sister Mjrn in the Henne Mines, releasing the beast Tiamat. It accompanied Judge Bergan at Mt. Bur-Omisace, endowing him with power. It is unknown if the slaughter of the war refugees at the mountain was entirely Bergan's doing, or if he was influenced by Venat as Mjrn was. Balthier first mentions Venat by name at the Phon Coast when he reflects on his past to Ashe, but cannot properly recall its name and calls it "Eynah".
At Draklor, the party confronts Cid with the sky pirate Reddas, where Venat tells Cid about Ashe's identity and he battles them as a "trial". Though Cid is defeated, Venat protects him as Reddas moves to strike him down, Cid calling to Venat by name and revealing the identity of the "shadow" they have seen. Cid invites Ashe to Giruvegan, telling her she can find a piece of nethicite there and he plans to go there as well.
At the Great Crystal, Ashe meets with the Occuria, who grant her the Treaty Blade to cut shards of nethicite from the Sun-Cryst. They tell her of Venat's "heresy" and to use the nethicite to destroy him and correct the "damage" he has done to history. Venat was tracking the party's actions, as it tells Cid about Ashe receiving the Treaty Blade shortly after it occurs.
At the Pharos at Ridorana, Cid and Venat appear after Gabranth fails to slay the party, Cid dismissing Gabranth and Venat protecting him when an angered Gabranth attempts to strike him. Cid has Venat re-integrate the Dusk Shard, Dawn Shard and Midlight Shard into the Sun-Cryst, spilling abundant Mist over Ivalice and awakening Cid's ultimate weapon and Vayne's command airship, the Sky Fortress Bahamut. Cid battles the party empowered with Mist and nethicite, but is defeated. Approached by Balthier, Venat moves to defend Cid but Cid tells it to let him pass, his life fading. With the Sun-Cryst's Mist out of control, Reddas destroys it with the Sword of Kings.
With Cid dead, Venat accompanies Vayne aboard the Bahamut. The party confronts Vayne during a battle between the Empire and the Resistance, Vayne using the power of nethicite to become Vayne Novus. With Vayne mortally wounded by Gabranth, Vaan attempts to kill him but Venat protects Vayne as he stumbles out onto the superstructure of the Bahamut's Mist cannon.
Apologizing to Venat for his failure to accomplish its goals, Venat comforts Vayne he has not failed, and tells him he shall not face death alone. Venat and Vayne merge, Venat creating copious amounts of Mist around them and fusing parts of the Bahamut onto Vayne's body, creating The Undying. The party destroys The Undying, causing Vayne and Venat to explode in a burst of Mist.