- God (originally) - As their creator/father, he governed the celestial race before abandoning them due to Lucifer's fall. He was said to eventually return by the angel Joshua. Something that has since come true.
- Michael (formerly) - When God left, Michael being the oldest Archangel, took control of Heaven. However when he fell into the Cage, he effectively lost all authority in the Host of Heaven.
- Raphael (deceased) - With Michael in the cage, he wanted the Host of Heaven to bow down to him and alluded to himself as being God.
- Castiel (temporarily) - Empowered by all the souls of Purgatory, Castiel, for a time, was able to rule Heaven with ease.
- Metatron (deceased) - As the scribe of God, Metatron knew of a spell that would cast out all angels from Heaven. After tricking Castiel into gathering the ingredients and stealing his grace, Metatron was able to use the spell and become the ruler and sole angel in Heaven. He lost this post after he was overthrown by the angels and later turned into a human by Castiel.
- Hannah (deceased) - Hannah was democratically elected by the Host of Heaven to lead the transition back to peace. Her leadership of Heaven ended when she was killed by the angel Efram.
- Lucifer (deceased) - After The Death of Hannah, Lucifer claimed the throne briefly in order to unite all the angels against the Darkness. In Season 13, the angels made him the 'undisputed Ruler of Heaven' after he promised he knew of a method to create new angels, and to restore all angels' wings, which turned out to be a lie.
- Naomi - Took charge of Heaven after Lucifer's departure.
- First Alternate Michael (erased) - He is the ruler of heaven in an alternate timeline where the angels abandoned the Earth.
- Second Alternate Michael (deceased) - He was the ruler of Heaven and commanded the angels in Apocalypse World.
- Michael (deceased) - God's oldest angel. After God left, he ruled in his place for at least 6 millennia as the general of the host. Following his imprisonment in Lucifer's Cage, he lost leadership of Heaven. After ten years, he was eventually freed when God opened all the doors in Hell. Michael was later killed by God when he briefly sided with the Winchesters in their efforts to defeat God.
- Lucifer (rebelled/deceased) - Before disobeying God, Lucifer was an extremely powerful force in God's heavenly alliance, serving as the lieutenant, and his most beloved angel. But since his fallout, he isn't part of the host anymore. However, he allied with the Heavenly Host briefly in order to stop the Darkness. Lucifer was severely weakened following most of his grace being stolen by an alternate reality Michael. He was later killed by Dean Winchester who was being possessed by alternate Michael.
- Raphael (deceased) - Before Lucifer's banishment, Raphael was an executive angel, whose initial designated ranking is unknown, although it is known that he watched over prophets. Once Lucifer was banished, Raphael fell directly under Michael. He took over for Michael after he fell into Lucifer's Cage and waged a civil war with Castiel for control over Heaven that ended with Castiel killing him and his followers.
- Gabriel (deceased) - A high-ranking executive angel, his actual ranking is unclear. He masqueraded as the trickster Loki on Earth. He was thought to have been killed by Lucifer with his own archangel blade, but later appeared alive in Season 13, explaining that he faked his own death by conjuring a duplicate that Lucifer stabbed. He later had his grace diminished, but remained quite powerful nonetheless (able to effortlessly kill a Prince of Hell empowered with some of his own grace). He was later killed by alternate Michael on alternate Earth.
- Tamiel (deceased) - A Grigori who spent millennia on Earth feeding off of human souls. As the angels believed the Grigori were wiped out, no one came after him, even after the Fall. However, his actions caught the attention of the Winchesters and the Seraph Castiel after he kidnapped and fed on the soul of Amelia Novak, the wife of Castiel's vessel, Jimmy Novak. Castiel and the Winchesters rescued Amelia, though she was killed in the process and Tamiel was killed by Claire Novak with his own angel sword.
- Akobel (deceased) - He was a seraph of the sixth choir that was sent to watch humanity. He was killed by Ishim in 1901 after being falsely accused of conceiving a nephilim.
- Castiel (promoted) - Castiel was the captain of his garrison that succeeded Anna. He was for the most part a very obedient/committed angel. But ever since he banished his superior, Zachariah, he was unable to return to Heaven. After being resurrected by God for a second time, he was promoted to the rank of Seraph and gained great power and influence over the angels of Heaven. He used this to start a civil war against Raphael that ended when Castiel declared himself the new God and smote Raphael and his followers. Castiel was ruler of Heaven for a time as the new God, but eventually gave up the power and died as a result of possession by the Leviathans. Even though he was resurrected again, he has chosen not to return to Heaven and has essentially renounced his role in Heaven, though he remains a Seraph and as such retains all of his powers. Castiel was later tricked by Metatron into helping him with a spell to expel all angels from Heaven and part of it was his Grace was stolen, rendering him human. After freeing Metatron, the host considered Castiel as a threat but he eventually formed a brief alliance with the angels in order to defeat the Darkness.
- Naomi - An angel of high ranking who existed in a part of Heaven that not many have been to. Metatron described her to be one of the key players in the power vacuum left by the Apocalypse and Castiel's self-proclamation as the new God. She could easily exert control to lower angels and even alter their memory. She was able to make Castiel answer her questions and able to order an incursion into Purgatory to rescue him that cost many angels their lives. She had several angels working under this division. After Castiel broke free of her control through the power of the Angel Tablet, she aided the Winchesters in finishing the second Trial, but repented after learning of Metatron's plans. After failing to stop him, Naomi appeared to be killed by Metatron with her own torture implement but later revealed that she is still alive.
- Bartholomew (deceased) - Naomi's former apprentice. After the angels had been cast out of Heaven, he assembled his own faction of angels, wishing to gather enough strength to retake Heaven. He attempted to recruit the seraph Castiel but, his recruitment became violent and he was killed by Castiel.
- Ion (deceased) - An angel that worked for Naomi and aided her in finding Castiel, but actually betrayed her against Crowley as he was disillusioned with Naomi and Heaven. He was killed by Castiel with one of Crowley's Angel Blade bullets in order to escape.
- Esper (deceased)
- Unnamed Angel
- Abner (deceased) - An angel that was imprisoned in Heaven's dungeon and a close friend of Gadreel. He was killed by Gadreel under Metatron's orders.
- Ambriel - An angel sent to Earth to check on The Darkness, and was promptly consumed.
- Anna (fallen/deceased) - She was originally a garrison leader, over Castiel, Uriel, and Balthazar. But when she fell and lost her Grace, that position was filled by Castiel. She eventually did reclaim her Grace, but she was later killed by Michael, burning her to ashes for trying to kill Mary Winchester before Sam and Dean were born.
- Balthazar (deceased) - Balthazar was a dear old and good friend of Castiel, fighting alongside him in the Host. Balthazar was "a great and honorable soldier", according to Castiel. At the first chance Balthazar got, however, he quit the Host, involving himself in Earth's song; wine, thievery, etc. At one point after Michael and Lucifer were imprisoned, he moonlighted as a Crossroads Demon on Earth. After helping Castiel a few times, he rejoined Castiel's forces. He was later killed by Castiel for betraying him.
- Uriel (deceased) - An angel that once served below Anna and Castiel, and was the replacement of Castiel after their superiors noticed that he was getting too close to humans. Castiel noted him as a Specialist, the meaning of which is unclear. However, he was a considerably powerful angel given his type. He was killed by Anna to save Castiel after being revealed to be a Lucifer loyalist.
- Zachariah (deceased) - Zachariah was the direct superior of Castiel and the subordinate of the archangels. He was an angel of high esteem, and largely recognized for his accomplishments and achievements, having worked for the archangels for six millennia. After his constant failure to secure Dean, Michael kicked him out, but decided to give him one more chance. By using Adam Milligan (the Winchester's half-brother), he drew the Winchesters into a trap, but was killed by Dean with an angel blade after he pretended to finally say "Yes".
- Rachel (deceased) - Her official ranking is unknown, however when Castiel rebelled, and formed his own battalion of angels, Rachel was his lieutenant and friend. She was killed by Castiel in self-defense when she betrayed Castiel and joined Raphael's forces.
- Hester (deceased) - Though she is only an average angel from Castiel's garrison, Hester assumed command of the Heavenly Host when Castiel and Raphael both died. She was killed by Meg to save Castiel.
- Inias - Average ranking angel from Castiel's former garrison who seemed to act as Hester's second in command. More forgiving of Castiel for his actions and more friendly to humans. He took over Hester's role after she died, but it is unknown if he remains alive as most of the angels from Castiel's garrison were wiped out by the Leviathans.
- Samandriel (deceased) - An angel that attended the auction in order to obtain and secure the Demon Tablet. He was killed by Castiel under Naomi's compulsion for revealing the angel tablet's existence.
- Hael (deceased) - Hael was a low-level angel who used terrakinesis to carve out the Grand Canyon, she was an angel that met Castiel after the Fall and was later killed by him when she threatened to alert other angels of his location.
- Malachi (deceased) - An angel that Castiel described as an "anarchist." After falling from Heaven he formed his own faction and went to war with Bartholomew for rule of Heaven. He was killed by Gadreel for not falling in line with Metatron's plans.
- Theo (deceased) - An angel that worked for Malachi as his torturer but secretly wanted to defect to Metatron as he found Malachi to be insane. After being tricked by Castiel, Castiel stole Theo's Grace to become an angel once more and then smote the now-human Theo with his own powers.
- Muriel (deceased) - An angel that remained neutral in the war between Bartholomew and Malachi but was captured by Malachi while telling Castiel about the war. She was killed by Theo while trying to make Castiel talk.
- Thaddeus (deceased) - An angel that was the torturer and the guardian of Heaven's dungeon before the fall. He was killed by Gadreel under Metatron's orders.
- Hannah (deceased) - An angel that was ambushed by Gadreel and became Castiel's second-in-command after he took up leadership of the angels against Metatron. Eventually turned against Castiel by Metatron's lies and helped capture him when he infiltrated Heaven with Gadreel's help, but switched sides after Gadreel sacrificed himself. She then insisted in the capture of Metatron. After returning to Heaven, Hannah was elected as leader of the Host. She was later killed by Efram for trying to Castiel.
- Ingrid - Low-level angel that acted as one of Metatron's assistants and was loyal to him even before he tricked Castiel's followers. Changed sides after Castiel broadcast the truth about Metatron over "angel radio." Later brings Metatron to Earth for Castiel at his request as she is one of the angels who like Castiel believes deeply in the mission to protect humanity at all costs.
- Nithael (deceased) - An angel dispatched to Earth after The Darkness' rising, who was killed by Lucifer.
- Ephraim (deceased) - After falling to Earth, Ephraim gained a vessel in the form of a man who had recently become deeply religious and a follower of the Reverend Buddy Boyle. Not understanding the ebb and flow of human pain due to his lack of interaction with humanity, Ephraim began a crusade to rid the world of pain by smiting those who were in pain. Ephraim eventually tracked Castiel's deep pain to a house where he was babysitting and confronted him. Ephraim confronted him to tell him that he should be trying to help the angels get back into Heaven and prepared to smite him. He felt that by remaining human, Castiel had already given up. Dean, who had figured out what Ephraim was up to, arrived and tried to stop him, but failed and Ephraim began to smite Castiel. However, Dean slid Castiel an angel blade and he killed the rit zien with it.
- Cupids - A special class of angels, they rank below other members of the Host. They are tasked in causing specific couples and bloodlines to meet and mix, depending on Heaven's interests. John Winchester and Mary Campbell pairing was a high priority for the Cupids.
- Secretarial angels - As described by Metatron as "run-of-the-mill" angels who functioned separately from soldier angels and intelligence angels
- Joshua (deceased) - He was significantly in a lower position than Zachariah however he has an important occupation, in cleaning/monitoring God's Throne Room, which appears as a garden, and he was the only one who God speaks to directly, albeit not face to face. During the crisis of Lucifer's Nephilim son, Joshua took the lead in dealing with the problem. He was killed by the Prince of Hell Dagon while trying to bring the Nephilim and his mother through the Heavenly Portal to destroy the child.
- Virgil (trapped) - "Weapons Keeper of Heaven". Sometime after his creation, he was put in charge of all of Heaven's weapons. He was considered to be the "nastiest" angel under Raphael's command. He is now trapped in a alternate Earth.
- Metatron (deceased) - The Scribe of God. An angel who was selected from the secretarial pool to be elevated as the Scribe of God. He left Heaven when the Archangels took over and cut himself off completely but retains all of his powers. He was recently responsible for banishing every angel to the Earth. After being exposed by Castiel, he was imprisoned in Heaven's dungeon, but Castiel freed him afterwards and stole his grace which turn him into a human. He convinced God to return was killed by the Darkness while helping to rescue Lucifer from her clutches.
- Gadreel (deceased) - As God's most trusted angel, Gadreel was chosen by God to protect the Garden of Eden but failed his task and was imprisoned since the dawn of time. He fell to Earth by Metatron's spell. After Dean Winchester prayed for help to save his brother, Gadreel took him as a vessel and acted as an ally of the Winchesters while secretly healing Sam of the damage from the Trials of God. After agreeing to become Metatron's second-in-command to rebuild Heaven, he murdered Kevin Tran and was expelled by Sam. Returning to his old vessel, Gadreel continued his work undaunted until Metatron's methods became too extreme for him and he defected to the Winchesters. After being imprisoned in Heaven once more, Gadreel killed himself with the Energy Focusing Sigil to release Castiel and help defeat Metatron.
- Anubis - Anubis is the Egyptian god of the dead and judgment. He ensures the dead go to their proper destination in the afterlife
- Atropos - Atropos is a Goddess of fate and destiny and is in charge of the inevitability of death along with her sisters, the Fates. They implement how mortals die.
For the first time in 2000 years, angels walked the earth. They sent angels to save the Dean Winchester from hell and to keep him from breaking the first of the 66 seals that would free Lucifer from his cage. They fought several skirmishes against demons, witches and other agents of Lilith. The host was also concerned with Sam's growing reliance on demon blood, and warned Dean that if he did not stop his brother, they would.
They sought to kill Anna Milton, a former garrison leader who chose to remove her grace to become human, to prevent her from divulging the plans of the angels and to prevent demons from taking hold of her and her ability to hear angels. Anna Milton eventually took her grace back to aid the Winchesters and Ruby in their fight against Alastair. She began to convince Castiel that the orders to usher the Apocalypse was not God's command.
During the battle for the seals, several angels were slain. In an effort to determine who was causing the deaths, as well as to halt the progress of hell in breaking open the seals, they captured Alastair. The angels forced Dean to torture information from the demon, who denied the accusations. It was later revealed that they died from the hands of their brethren, who were led by Uriel. The rogue angel wished to free Lucifer, because like the archangel, Uriel believed humans to be below angels, and only saw themselves as the perfect creation of God. Moments before Uriel was about to kill Castiel, Anna arrived and killed Uriel herself.
The revelation of Uriel's betrayal prompted Zachariah, the superior of the lower angels, to come down to earth. He convinced Dean about his purpose and the role he would play in the apocalypse. In truth, the higher angels actually wished to let the seals be broken so that their leader, Michael could finally vanquish Lucifer and usher paradise on earth. This ulterior motive guided most of the actions of the host, even threatening the prophet Chuck not to warn Sam and Dean of the impending result of the battle for the seals. Zachariah had Castiel captured and taken back to heaven for rehabilitation. Castiel went back to earth strictly adhering to Heaven's orders and had Anna Milton taken to Heaven as well. Zachariah and his angels also prevented Dean from reaching Sam in time before he could kill Lilith, whose death meant the final seal would be broken.
Castiel finally decided to act on his own accord and allowed Dean to get to Sam. Chuck had a vision of this and noted it was not supposed to happen. This prompted Raphael, who was tethered to the prophet, to arrive and to smite Castiel, who attempted to hold the archangel off. Castiel, however, stood no chance and was killed.
The host, led by Zachariah, scrambled to secure the Michael Sword. The prophet Chuck knew of the location, which he revealed to Dean to be inside John's Lock Up. Zachariah waited for Sam and Dean inside the locker, and revealed that the Michael Sword actually referred to Dean being the archangel's true vessel, and the prophecy Chuck shared was actually falsely implanted to lead the brothers to the angel. Dean, however, would not agree to being used as a vessel. This infuriated Zachariah, who threatened to harm the Winchesters, until Castiel's arrival prevented Zachariah from doing so. To protect the Winchesters, Castiel carved Enochian sigils on the ribs of the brothers, which hid them from all angels in existence, including Michael and Lucifer, who were both actively trying to reach their true vessels.
The Heavenly Host spent most of their efforts trying to secure the Winchesters, albeit to little effect. They continued to fight battles against demons, and other forces of hell, including the antichrist or the cambion, which could wipe out the Heavenly Host with a thought. Desperate, they resurrected Adam Milligan, half-brother of the Winchesters, as a contingent vessel for Michael. Sam and Dean convinced Adam to refuse, although the machinations of Zachariah proved to be effective. Although killed by Dean, Zachariah was able to secure consent and summon Michael. The archangel missed his true vessel, but decided to trap and take Adam instead.
Eventually, Lucifer secured a consent from Sam, and met with Michael to begin their battle. The rest of the host did not intervene, as they believed Michael was more than capable to defeat his brother, and that it was Michael's destiny to do so. Castiel, Dean and Bobby attempted to prevent the fight by causing diversions. Castiel banished Michael with Holy Fire, which angered Lucifer, who then killed Castiel. However, this bought enough time for Dean to talk to Sam and convince his brother to overpower Lucifer, moments before Michael returned. Sam and Dean managed to trap the archangels in Lucifer's Cage, effectively averting the apocalypse, and leaving the heavenly host leaderless. A newly resurrected Castiel was elevated as a seraph returned to Heaven to ensure order.
Shortly after the Apocalypse was stopped, Raphael called an assembly of the Host, in which angels would either align with him, or die. The archangel planned to restart the apocalypse. This drew opposition from Castiel, who started promoting free will among angels. Raphael did not like Castiel's insurrection and made it clear by demonstrating his power. Castiel then struck a deal with Crowley to prevent the archangel from pursuing his plans to restart the apocalypse. Crowley loaned Castiel with enough souls to challenge Raphael. At that point civil war has erupted, with angels taking either of the opposing sides.
Balthazar, a rogue angel, has stolen Heaven's weapons, which were sought by both of the belligerents. Balthazar loosely aligned himself with Castiel, which allowed the seraph to force even the archangel Raphael to flee.
Castiel, who sought more power from souls ordered Balthazar to save the Titanic, thus creating several thousands of souls to boost their power. However, this drew the ire of Atropos, who was willing to let the planned future go but was determined to keep the past the way it was supposed to be. After a stalemate, Castiel was forced to order Balthazar to correct the flow of events by sinking the Titanic again.
Meanwhile, as part of the deal with Crowley, Castiel secretly assisted in torturing monsters to locate Purgatory and use the monster souls to power themselves. This eventually became known to his lieutenant Rachel, who saw the partnership as unclean. She was distressed that she put her faith in someone who would work for a demon and attempted to kill Castiel. The fight between the two resulted into the death of Rachel.
Crowley and Castiel eventually discovered how to open Purgatory, but in the last minute, Castiel removed Crowley from the deal, claiming all the souls for himself. The angered demon then switched alliances and was given the protection of Raphael, who forced Castiel to surrender. However, the seraph tricked both the demon and the archangel and managed to absorb the souls from Purgatory. He then let the demon escape a few moments before smiting Raphael, effectively ending the war and the plans to restart the apocalypse.
After absorbing every soul in Purgatory, along with the Leviathans, Castiel, returned to Heaven and slaughtered any remaining angel who allied with Raphael during the civil war. This drastically reduced the number of the heavenly host, although this would not be the last massacre that the host would suffer from.
Later, two angels from his garrison, specifically Hester and Inias, came to Earth to secure the Prophet, Kevin Tran. Hester was killed, and Inias returned to Heaven, bringing the rest of the garrison under his leadership. Castiel revealed that his garrison and all the angels who were posted on the Earth were either hiding or dead as the Leviathans might have killed them all. It is unknown if any of the garrison survived or if Heaven has sent a new garrison to watch the Earth now that the leviathans are leaderless.
Heaven was still in disarray and heavily factionalized, with several angels vying for control. A group of angels under the command of the mysterious angel Naomi rescue Castiel from Purgatory. The incursion cost many angels their lives, but it was successful. Naomi later summoned Castiel to her and ordered him to report in to her on the Winchesters from time to time and to aid them in any way they need. Naomi's primary goal was to secure the Angel Tablet and to help the Winchesters close the gates of Hell.
Castiel successfully located the Angel Tablet but was released from Naomi's control upon his contact with the tablet. He fled and took the tablet with him, prompting Naomi to locate Castiel.
Metatron, the Scribe of God who was forced to exile himself from Heaven to protect the Words of God, was later located by the Winchesters. He helped the Winchesters in their goal to seal the gates of Hell. At the same time, he convinced Castiel that Heaven also needed to be shut so that angels could settle their disputes against each other and prevent their quarrels from bleeding into earth. He aided Castiel in completing the first two trials. However, before Castiel could finish, he was abducted by Naomi and her angels.
Naomi attempted to uncover Metatron's thoughts and discovered the scribe was actually working on a plan of vengeance against all the other angels. The trials he set Castiel to were actually part of a spell to banish all angels from Heaven. Naomi immediately conveyed this to Castiel, who was wary of Naomi, but was willing to listen. Castiel travelled to Heaven only to find Naomi "dead". He was then incapacitated by Metatron, who removed the seraph's grace and turned him into a human, thus completing the spell. Not long after, the entire Host of Heaven save for Metatron was seen falling down onto earth, losing their wings in the process.
After being cast from Heaven, the angels split into many factions, some neutral such as the Penitents and some, like Bartholomew's and Malachi's warring for rule over Heaven once they reclaim it. In order to fight better in the war, Castiel steals the grace of the angel Theo, restoring much of his powers and angelic status, but is no longer a Seraph.
Growing bored of being in Heaven alone, Metatron begins recruiting his own faction with the help of Gadreel to rebuild Heaven under his command. While initially loyal to and helping the Winchesters, the prospect of redeeming himself causes Gadreel to switch sides and murder Kevin Tran who Metatron makes sure is the last Prophet. Despite the setback of Sam Winchester expelling him from his body, Gadreel simply got a new vessel and continued his work for Metatron, amassing a massive following at least somewhat through force and intimidation. At the same time, Metatron used the Angel Tablet which Gadreel had brought him to attain Deity-like power by tapping into the tablet's power.
In the war that followed, Castiel killed Bartholomew in self-defense and Gadreel killed Malachi when he refused to join Metatron. With the two major faction leaders dead, their forces joined either Metatron or a faction Castiel created at the insistence of Metatron himself and an illusion of Gabriel to oppose him. Using brainwashed angel suicide bombers, Metatron managed to turn all the angels to his side, including Castiel's followers and the neutral factions and gained control of the whole surviving Host. However, Metatron's methods turned Gadreel against him and he sided with Castiel and the Winchesters to bring Metatron down.
Working together, Gadreel and Castiel infiltrated Heaven while Dean Winchester, armed with the Mark of Cain and The First Blade confronted Metatron on Earth where he was performing miracles to get humans to worship him instead of God. Thanks to Gadreel sacrificing himself, Castiel managed to turn his former second-in-command Hannah back to his side and locate and destroy the angel tablet, shattering Metatron's power and returning him to a normal angel, but not before he mortally wounded Dean who resurrected as a demon later as a result of his death and the Mark of Cain's power. Fleeing an attack by Sam Winchester to Heaven, Metatron confronted Castiel in his office, gloating about how even without his extra power he'd still be the leader of Heaven because the angels were "sheep" who would follow him and that he didn't think much of humanity either. Unknown to Metatron, Castiel used Metatron's own equipment to broadcast the conversation over "angel radio," turning the whole Host against him again. Angels stormed Metatron's office and captured him, but Castiel locked him in Heaven's dungeon rather than kill him. The angels have reclaimed Heaven, however, the Gates remain closed and it is only accessible by a portal.
Following Metatron's defeat, the angels reopened Heaven to all souls, though they still need to use Metatron's portal to enter and exit. Metatron was permanently locked in Heaven's dungeon and the angels began leading themselves, rebuilding Heaven and reconciling the differences between the factions that had popped up while on Earth. Its later stated that Hannah now leads Heaven and Heaven is in better shape than it has been since God left.
At Hannah's insistence, a dying Castiel aids her in her efforts to locate angels who don't want to return to Heaven and convince them to go back. With the help of Crowley, he restores himself once again using the grace of Adina and helps restore Dean to humanity. However, Hannah eventually returns to Heaven so that her vessel can resume a normal life. Castiel continues his search for other angels and even starts looking into his own vessel's family. Castiel also attempts to locate a cure for the Mark of Cain, briefly bringing in Metatron in hopes that he will know something and searching for Cain, the bearer of the Mark before Dean. After discovering that Cain has returned to his old ways, Castiel aids the Winchesters and Crowley in finally stopping the Father of Murder for good. An attempt to force Metatron to tell them how to cure the Mark of Cain leads to Castiel regaining his remaining grace and status as a Seraph, but Metatron, now human, escapes with the Demon Tablet and is on the loose once more.
While trying to help find Amelia Novak, his vessel's wife, Castiel learns of the survival of the Grigori, elite angels that became corrupt and were believed wiped out millennia ago. The Grigori are now feeding on human souls and one, Tamiel, has been feeding on Amelia's soul. Tamiel is killed by Claire Novak with his own angel sword, but it is unknown how many Grigori there still are out there.
Castiel later aids in the attempt to translate the Book of the Damned and remove the Mark of Cain. While they are successful in removing the Mark, their efforts unknowingly releases the Darkness, a primordial evil that God and his Archangels had locked away at the beginning of time. Castiel is also put under a spell by Rowena and is forced to attack Crowley.
Under the influence of Rowena's spell, Castiel attacks Crowley who escapes by smoking out. Castiel travels to the portal to Heaven for help only to find it gone. Learning of the Darkness release, Castiel prays to his siblings for help and Efram and Jonah respond and lead him to a warehouse, explaining that the angels moved the portal after Metatron's escape. However, they have no intention of taking Castiel to Heaven and instead chain him up and torture him repeatedly for information on Metatron. Finally, Hannah arrives and puts a stop to the torture, but is unable to heal Castiel or break Rowena's spell. Hannah informs Castiel that the alarms in Heaven have gone off for an unknown reason and Castiel informs her of the escape of the Darkness. Hannah asks him about the Winchesters location and Castiel realizes the whole thing is a trick in hopes of getting information out of him. Hannah explains that since he helped Metatron escape, most of the angels hate Castiel now and she is working under orders from the new democracy in charge of Heaven to find out what he knows. When Castiel refuses to cooperate, Efram and Jonah attempt to use a device similar to the one Crowley used to hack Samandriel and Gadreel to hack Castiel's brain. As Hannah distracts the other angels with her objections, Castiel falls back under the influence of Rowena's spell and breaks free, killing Jonah in self-defense. An angry Efram murders Hannah for her interference before Castiel kills him too. Castiel later travels to the Bunker to enlist Sam and Dean's help.
Afraid that Amara might destroy Heaven, the angels decide to do a unified smiting. Three angels were sent down to warn Amara that if she refuses to surrender, each and every angel in the skies is ready to smite her with one unified blow. After Amara kills the three angels, the remaining Host of Heaven throw down a beam powerful enough to weaken her enough that she needed the help of Rowena and The Book of the Damned to heal her.
The Host soon discovers their attempt was unsuccessful, and they make no further move to interfere with Amara. Lucifer, in possession of Castiel's vessel, comes to Heaven in hopes that they would join him in the battle against the Darkness. The angels are reluctant at first, but soon agree. Lucifer vanishes however when the Darkness kidnaps him for torture.
Thanks to the Winchesters, Lucifer escapes the Darkness and returns to Heaven once more to once again ask for help in battling the Darkness, this time as part of God's plan. The angels are hostile and untrustworthy, but Castiel convinces them to play their part as he has played his.
The Host summons another combined smiting and attacks Amara after her vessel was weakened by the witches. They presumably observe the battle and realize God's defeat at Amara's hands. This leads the Host to lock up Heaven and prepare for their end.
The still alive angel Naomi tells Castiel the status of the Host of Heaven. Heaven runs on the power and he number of angels still alive, and because their numbers have shrunk to barely a dozen angels, Heaven was barely running and she later decides to lock Heaven up.
After Jack Kline's death, the Shadow attacked Heaven in order to drag his essence into the Empty, injuring the angel Zuriel after having opened all gates of Heaven. However Castiel made a deal with the entity, persuading it to leave.