|“||The angels... they're falling.||”|
After the Prophet Kevin Tran is kidnapped by the King of Hell Crowley, the Winchesters track down angel and Scribe of God Metatron in Colorado where they enlisted his help to complete the Trials of God. After being informed of the situation in Heaven by the Winchesters, Metatron rescued Kevin and the angel and Prophet informed the Winchesters of the final Trial. However, unknown to the Winchesters and Kevin, Metatron was enraged at the fact that after God left Heaven, the archangels went after him for his knowledge of God, forcing Metatron to flee Heaven. Wanting revenge, Metatron becomes determined to expel all angels from Heaven and take rule of it for himself.
Having learned of Castiel from Kevin Tran, Metatron approaches Castiel for help with supposedly performing the Angel Trials to close up Heaven and force their siblings to reconcile their differences. Metatron is able to convince Castiel to do the "Trials" since Castiel blames himself for the state of Heaven. Metatron then reveals that the waitress, Jane, at the restaurant they are located at is the first "Trial": cut out the heart of a Nephilim. Castiel reluctantly agrees to help Metatron kill Jane.
Metatron and Castiel corner Jane who is able to tell what they really are. Though Jane pleads with them to let her live, Castiel refuses and the two angels engage in a fight with the Nephilim. However, Jane is stronger than both of them put together. Finally, Castiel stabs Jane through the neck with an angel blade while she is distracted with Metatron, killing her.
Next, Castiel and Metatron travel to Houston, Texas where Metatron informs Castiel that the next "Trial" is to get a Cupid's bow and he learned from angel radio that a man named Dwight Charles is the next on the Cupid list to fall in love. Metatron assures Castiel that unlike with Jane, there is no need for killing this time. As the two wait for Cupid to arrive in Dwight's bar, Naomi arrives with two angels to capture Metatron, having learned that he and Castiel had been spotted from Nathaniel. The angels capture Metatron and start to attack Castiel, but after Dwight shoots one, they leave without a further fight.
Taking Metatron to Heaven, Naomi starts to torture him with her drill for God's secrets. Probing Metatron's mind, Naomi discovers his true plan and demands to know why he's doing it. Metatron explains that he wants revenge for being driven from his home and Naomi takes off to stop Castiel from making a mistake.
Needing help after Metatron's capture, Castiel turns to Dean to help him complete the "Trials." At Sam's insistence, Dean goes with Castiel to complete the "Trials" while Sam completes the third Demon Trial by curing Crowley. Dean and Castiel bring Kevin the angel tablet in hopes he can translate the Trials from it for them. Although Kevin is reluctant, Castiel gets him to do it.
Returning to the bar, Dean and Castiel keep an eye out for the Cupid and Dwight's match. Eventually a woman named Gail arrives, but there ends up being no connection between her and Dwight. Moments after she leaves, Dwight and his regular customer Rod show an attraction to each other and Dean and Castiel realize that Gail was the Cupid. Dean and Castiel later confront Gail and Dean convinces Castiel to talk to Gail before forcing her to give up her bow. After Castiel reveals what he intends to do, Gail admits that she's afraid to go home due to the chaos in Heaven and willingly offers Castiel her bow since he believes he can use it to fix Heaven.
After getting the bow, Dean calls Kevin who tells him he located the Angel Trials but didn't see anything about a Nephilim's heart of a Cupid's bow. As Dean tries to get Kevin to keep looking, Naomi arrives, insisting she's there to talk, not fight. Naomi tells Castiel that Metatron lied and he isn't trying to fix Heaven, but break it. While Castiel refuses to listen due to Naomi's past with him, Dean gets Castiel to hear her out. Naomi explains that Metatron intends to expel all angels from Heaven onto Earth like God had cast out Lucifer. Naomi admits she doesn't know where the angels lost sight of their mission to protect humanity and tells Dean that if Sam completes the Trials he will die. She then tells Castiel that if he truly wants back in, she will listen and begs him to stop his path as Metatron has been neutralized. Kevin is unable to confirm Naomi's story one way or another from the angel tablet but Dean has Castiel return him to the church where Sam is nearly finished curing Crowley. Castiel refuses to believe Naomi was telling the truth and returns to Heaven to find out for himself.
In Naomi's office, Castiel finds her dead with her torture drill impaled in the back of her head. Metatron holds an angel blade to his throat and reveals that Naomi had been telling the truth. Metatron restrains Castiel in Naomi's torture chair and tells him that what they had been doing was never Trials but collecting the ingredients for a spell. Metatron tells Castiel that the last ingredient is Castiel's grace and takes it from him, rendering Castiel human. Telling Castiel to enjoy his human life, Metatron teleports him back to Earth.
Shortly after Castiel is sent back to Earth, the angels start to fall as witnessed across the world as an apparent meteor shower while Sam, Dean, Crowley and Castiel watch it from their various positions. The Fall also lights up the bunker's computer which Kevin witnesses. All over the world the angels fall to Earth with many being without vessels and left in confusion while others are injured. Many angels die including Sophia, Azrael and Ezekiel. The Fall affects all angels in Heaven including imprisoned angels such as Abner and Gadreel who Fall as well.
Following the Fall, the angels were initially left in confusion, but quickly began organizing into factions. After growing bored of being alone in Heaven, Metatron decided to bring the angels back under his rule with Gadreel as his second-in-command. He eventually gets his hands on the angel and demon tablets and uses the angel tablet to gain Deity-like abilities. Eventually, Metatron is overthrown thanks to the efforts of Castiel, Gadreel and the Winchesters and the angels reclaim Heaven. However, the Gates remain closed even after Heaven is reclaimed and the angels are forced to rely on Metatron's portal to get in and out of Heaven.
After Castiel's grace is stolen, he spends several months as a human. Shortly after the Fall, the angels of Bartholomew's Faction begin hunting for him, but are foiled in their attempts. Following an encounter with the angel Ephraim, Castiel begins actively looking for a way to restore the angels to Heaven. To this end, he steals the grace of the angel Theo and regains his status as an angel. However, the stolen grace quickly begins burning out though it holds long enough for Castiel to defeat Metatron and reclaim Heaven. He eventually gets Adina's grace to replace it with the help of Crowley before he reclaims the remains of his original grace and regains his full power.
Several years later, it was revealed that Naomi had actually survived Metatron's attempt to kill her. However, it took her years to recover from the attack and used a few reliable angels to spread the news of her "death."
- This event leaves Castiel human for a time before he steals Theo's grace. Unlike the other angels, Castiel is able to adapt well to the human world, enough to survive for months on his own before becoming an angel once more.
- In War of the Worlds, over four years after the Fall, the angel Duma tells Castiel that the Fall has left the angels nearly extinct due to the number of angels killed in it.
- In Devil's Bargain, Lucifer claims to know a way of fixing the angel's wings and creating new angels. Later it has been found out that he lied.
- It is assumed that after Jack Kline becomes the New God, he restores the angels’ wings. This is not shown but can be deduced from Bobby Singer’s statement in the finale, saying Jack “made some changes” before he left.