After the Battle for Eden and the resulting Damocles Event, Wonkru was forced to leave Earth and go into space, where they began their new journey across the stars. They eventually found a new home in Sanctum. Despite this, Earth has regenerated and become habitable again, leading John Murphy to advocate for Wonkru and the other people in Sanctum to go to Earth.
With the death wave approaching, the Grounders and Sky People decided that control of the Second Dawn Bunker would be decided by a Final Conclave. Octavia Blake won the Conclave but instead of just leading Skaikru into the bunker, she decided that the remaining clans would form into a single clan, known as "Wonkru" ("One Clan" in Trigedasleng), and share the bunker equally. Thus, 100 members from each surviving clan (excluding Floukru, who all had died) were ushered into the bunker to survive.
At first, Octavia ruled over Wonkru as Osleya (Champion in Trigedasleng) with a council consisting of a delegate from each of the clans. However, after nearly two months of relative (albeit tense) quiet, part of Skaikru led by Kara Cooper rebelled against Octavia and barricaded themselves inside the bunker's cafeteria, isolating the rest of the people from their food source. This led to massive chaos in the rest of the bunker. Octavia, advised by Thelonious Jaha, reinforced the union of the clans by killing those who dared oppose her.
After the rebellion was thwarted, Octavia took full control of Wonkru and became known as Blodreina ("Red Queen" in Trigedasleng). Anyone who committed any crime was considered an enemy of Wonkru. Justice was then served via gladiatorial fights to the death, with the winner possibly earning their freedom.
About two years after Praimfaya, a fungus devastated the soybean plants. Cooper was able to isolate a few healthy plants but said that it would take a year before the farm would recover enough to support the bunker's population. Without a proper source of protein, people would die of malnutrition, so Abby Griffin proposed a grim solution: Eating those that died in the fighting pits. However, in the mess hall, Marcus Kane tells everyone that they have a choice not to eat. Afterwards, Abby tells Octavia that to survive they must have full compliance, citing the Blight Generation on the Ark to describe what happens if they don't. To gain said compliance, they must make refusing to eat a crime. At first, Octavia objects to killing her own people, but then grudgingly agrees with Abby that there is no other choice. The next time people refuse to eat, Octavia begins to kill three of them, until Kane and the other resistors agreed to eat. Wonkru calls this year of cannibalism – their second overall year in the bunker – "The Dark Year", named for the serious emotional repercussions left on Wonkru as a whole.
During the six years in the bunker, the population was reduced from approximately 1,200 people to 814. In other words, approximately 386 people died during those six years of Octavia's rule.
Six years after Praimfaya, the Eligius prisoners open the bunker after making a deal with Bellamy Blake. The prisoners lift everyone out of the bunker, but then betray the group by claiming the Shallow Valley as their own and demanding Abby Griffin because they need a doctor. Abby agrees to come willing if they take Marcus Kane as well, since Octavia is holding him prisoner to fight in the gladiatorial matches. After the prisoners leave, Wonkru declares war on them, thus starting the Battle for Eden.
Octavia sets out across the desert with a battalion of soldiers, but parasitic worms and a sandstorm hamper their progress towards the valley. Monty warns them of incoming missiles, and later that night, the Gagarin fires a missile at the Wonkru campsite. However the campsite is empty, since the battalion retreated into the sandstorm. Between the worms and sandstorm, Wonkru returns to Polis with twelve dead.
Later, the Gagarin drops food supplies and a message in Polis. Diyoza tells Wonkru that they can defect from Octavia's leadership and join her at Shallow Valley. Octavia sends Echo to infiltrate the Eligius camp to get access to the ship's computer by posing as a Wonkru defector. That evening, several real defectors join Echo to escape Polis and board the Gagarin. However, Kara Cooper, on Octavia's orders, shots at the defectors, killing several of them.
Within the bunker, Octavia and Cooper begin experimenting with the parasitic worms. They hope to use the worms as bio-weapons against the prisoners in the valley. Cooper, without telling Octavia, infects a surviving defector to study the effect on a live body. Clarke, Bellamy, and Indra sabotage the plans by using the worms to kill Cooper and destroying the worms. However, Octavia sees through the ruse and has Clarke arrested for Cooper's murder.
To prevent Clarke's execution, Bellamy puts Octavia in a coma to prevent her from executing Clarke. Bellamy and Indra plan to have Madi take the Flame so she can become the Commander of Wonkru. Octavia awakens but Indra locks her away, while Gaia successfully inserts the Flame. However, before the ascension ceremony can be completed, Clarke releases Octavia. Octavia has Gaia, Indra, and Bellamy arrested, while Clarke and Madi escape in the rover.
Gaia, Indra, and Bellamy are forced to fight in the arena, but Monty and Harper interrupt. Monty reveals that the hydrofarm is working again and they don't need the valley. After Wonkru begins to rebel against her, Octavia burns down the farm, leaving them no choice but to march with her towards the valley.
During their travels, Echo contacted Bellamy with intelligence on the Eligius prisoners' battle plans. Bellamy offers Octavia the information if she agrees to his terms: to accept the prisoners' surrender with no executions or fighting pits, but real peace. Octavia agrees and the two plan for battle.
Four days later, the Wonkru soldiers enter a gorge at the edge of the valley. However, the prisoners are ready and massacre them. Unbeknownst to Wonkru, Kane and Diyoza, who had been with Echo, revealed Wonkru's plans to McCreary. Some Wonkru survivors are able to retreat back to their desert campsite, and Madi with three others rescue Octavia, Bellamy, Indra, and Gaia.
Back in the desert, Octavia relinquishes control of Wonkru to Madi, allowing her to officially become the Commander of Wonkru. The Flame helps Madi create a plan and they successfully invade the valley. The prisoners surrender, and because of this, Bellamy convinces Madi not to kill them and to break the cycle of deaths. However, McCreary refuses to surrender and deploys the Damocles bomb, before he is killed by Clarke. Everyone is forced to flee onto the Gagarin to escape to space and the bomb destroys the valley.
In space, they board Eligius IV and decide to go into cryosleep for ten years while Earth recovers. However, Earth remains barren, so Monty Green extends the cryosleep while he searches for a solution. After 125 years in cryosleep, Wonkru arrives to a new habitable world.
After the arrival at Sanctum, the majority of Wonkru was left in cryo while a select few were woken up to explore the new world and make arrangements for possible settlement. After Madi fell under the influence of Sheidheda, concern grew that she would return to the ship and awaken Wonkru, effectively putting the entire army under the control of the insane Dark Commander through Madi.
The Primes later hijacked Eligius IV and decided to mind wipe the entire sleeping Wonkru to be their future hosts, which would effectively kill them all. Clarke Griffin, posing as Josephine Lightbourne, attempted to talk the Primes out of this, but was forced to break her cover to prevent this genocide. After all of the other Primes were floated by Clarke, Russell and the Sheidheda-possessed Madi awakened most if not all of Wonkru which followed their Commander in turning against Clarke and her friends. After Clarke was about to commit suicide, Madi regained control and ordered Wonkru to arrest Russell and his guards instead. Shortly thereafter, Raven was forced to delete the Flame to save Madi from Sheidheda, making Madi no longer the Commander.
After the overthrow of the Primes, Wonkru tries to keep the peace between different factions in Sanctum. To keep the Flame's destruction a secret, Indra is a de facto leader and speaks for the Commander, pretending that Madi Griffin is still "Heda".
Due to the threat of a nuclear meltdown, Indra asks Wonkru for help, claiming that the Commander orders them to do it. However, Knight, a former member of Sangedakru, is suspicious and begins questioning Indra's secret, but Gaia reveals the truth that she destroyed the Flame to stop Sheidheda. Because of this, Wonkru refuses to go into their deaths in the nuclear reactor. Despite Wonkru calling off-duty to live their normal lives in Sanctum, at least some Wonkru members decide to help Indra and the others with their plans of executing "Russell Lightbourne". After some of the Wonkru members begin bringing Russell (who is actually Sheidheda in disguise) to calm the citizens and to announce that he will accept his execution, an assassin shoots him, forcing a small amount of Wonkru members to bring "Russell" to Medical. Without the assistance of Wonkru, those remaining loyal to the cause find it harder and harder to deal with difficult tasks.
With the situation getting progressively worse and terrified that the resurrected Sheidheda will gain control of Wonkru, Indra attempts to get Madi Griffin to resume her role as Commander of Wonkru. However, Madi proves to be too terrified and runs off. Instead, John Murphy and Emori suggests that Indra take control of Wonkru herself, pointing out that in the bunker, Indra was the true power behind the clan. Though Indra is reluctant, the two convince her to take control. Indra declares to the gathered Wonkru that there are no more Commanders and she is now the leader of the united clans. Though Knight challenges Indra, she easily defeats the Sangedakru warrior and gives a rousing speech, reuniting Wonkru under her leadership.
After Sheidheda reveals his identity to Wonkru, Indra challenges him to a single combat for control over the clan. He accepts, and although he initially wins the fights, Sheidheda is badly injured after Madi stabs him in the eye. Indra promises to kneel to the Dark Commander if he spares Madi's life. Indra kneels to Sheidheda, and he assumes control of Wonkru. Now in control of the whole of Sanctum, Sheidheda forces the other factions in Sanctum to kneel to him or die. Nikki and the prisoners kneel, but Nelson and the Children of Gabriel refuse and are all massacred, apart from Luca who is saved by Indra.
In "Praimfaya", when the bunker is sealed, there are 1,200 living members of Wonkru.
By "Pandora's Box", there are only 814 members of Wonkru remaining. Abby and Kane's decision to get into Charmaine Diyoza's ship peacefully makes them enemies of Wonkru, and twelve other members die in "Shifting Sands", leaving 800.
In "Exit Wounds", Octavia makes Madi a member of Wonkru, but an unknown number of defectors manage to reach the Gagarin transport ship, and others are killed by Kara Cooper, further decreasing Wonkru's numbers.
In "Sic Semper Tyrannis", Octavia learns that Bellamy, Indra and Gaia have betrayed her, and so she makes them enemies of Wonkru as a whole. As of this episode, there are about 770 members of Wonkru.
As of "Damocles (Part 1)", approximately 300 members of Wonkru were left alive after the initial failed attempt to invade Shallow Valley. Some of them, who were branded as traitors of Wonkru, later rejoined the clan, with Madi as their new Commander.
In "From the Ashes" we learn that only 36 Eligius prisoners survived the conflict with Wonkru so starting with the original number of people that left Earth (411) and subtracting Clarke, Madi, Spacekru (5), Jordan, Eligius (36 + Shaw and Diyoza), Kane, Abby and the Wonkru members that died in "The Blood of Sanctum" (5). We can calculate that there are 358 members of Wonkru left.
After Kara Cooper's rebellion was prevented, Octavia took full control of Wonkru and became Blodreina ("Red Queen" in Trigedasleng). The title Blodreina is derived from a moment when Gaia became willing to accept Octavia as her leader and showed Octavia her bloodied figure in a mirror, stating that the blood of Wonkru's enemies was Octavia's armor, and thus an extension of her.
As revealed in "Nakara," while Octavia was in charge of Wonkru as the sole leader, it was in fact Indra who kept things going from behind the scenes and was in essence the true power in the clan in the more mundane matters.
In "Damocles (Part 2)," Octavia gave up power completely to Madi Griffin, the new Commander, symbolically becoming the first to bow to her after recognizing just how far wrong her own leadership went.
In "What You Take With You," though no longer the leader of or even part of Wonkru, having been exiled by Bellamy, a repentant Octavia gave up the title of Blodreina for good.
In "Damocles (Part 2)", Madi Griffin became officially Heda of Wonkru as Octavia sticks her sword to the ground and kneels down and bows before her, recognizing her as the Commander.
In "The Blood of Sanctum", Raven deletes the Flame which is then removed by Eric Jackson to save Madi's life. As a result, Madi is no longer the Commander of Wonkru.
In "Nakara", Sheidheda suggests that Indra needs a Commander to reunite the fractured Wonkru. The Dark Commander suggests that Clarke, having borne the Flame briefly, could take the job, but knows that Indra fears that Wonkru will choose to follow him instead as a former Commander. Indra later admits that Sangedakru at least would follow the Dark Commander if the truth ever came out and believes that in time the rest of Wonkru would as well. In response, Indra attempts to make Madi the Commander again to reunite the fractured Wonkru, but Madi refuses as she is too afraid. Instead, Indra takes complete command herself and orders John Murphy and Emori to dispose of the emblem the Commanders wear on their foreheads instead of donning it herself.
In "A Little Sacrifice", Sheidheda takes control of Wonkru and becomes Commander again, forcing Murphy, Emori, Madi, and the others to prepare to fight back against the Dark Commander's reign.
After the Flame is removed from Madi and she is no longer fit to lead Wonkru, Indra and Clarke take over as co-leaders though they keep the clan in the dark about the truth and pretend that they are passing on orders from Madi herself. However, this falls apart in "False Gods" when Wonkru learns that the Flame has been destroyed and most abandon the cause. The few that remain continue following the leadership of Clarke and Indra and then Indra alone after Clarke leaves in "Hesperides."
In "Nakara," the mounting threat from the Eligius prisoners and Sheidheda causes Indra to attempt to make Madi the Commander again. When this fails, John Murphy and Emori convince Indra, who they recognize was the true power behind Wonkru while they were in the Second Dawn Bunker, to take full command of the clan herself. Indra asserts her leadership to a gathering of Wonkru stating that while there are no more Commanders, having had Murphy and Emori get rid of the Commander emblem to emphasis her point, Indra is in command. Though Knight challenges this, Indra effortlessly defeats the dissenting Sangedakru warrior and rallies Wonkru behind her with an inspiring speech.
After Kara Cooper staged an unsuccessful coup with some other former Skaikru members to take the food supply for themselves, Kara, her fellow Skaikru accomplices, and other Grounder criminals were consequently punished for their decisions. This punishment, handed down by their new leader, Octavia Blake, was that of a gladiatorial fight for freedom, where only one indvidual emerged as the champion by being the last person standing. This event triggered the initiation of an institutionalized punishment system inspired by Bellamy's book about Ancient Rome, which he read to his sister Octavia as a child.
This method of punishment was later abandoned once Wonkru had left the Second Dawn Bunker.