Nanael is reassigned by the Head Angel to compete in the Queen's Blade as punishment for failing her prior assignment. Heaven suspects something is wrong with Queen Aldra. Everyone is looking for residences in Gynos: Tomoe with Shizuka, Ymir with Cattleya, Alleyne with Nowa, Nanael with Melpha, and Elina with Claudette. Echidna is there as well, and confronts the rogue assassin Irma. Melona tries to take things into her own hands and assassinate Aldra, but is turned to stone by Aldra's power. Nyx, a new contender, is revealed.

Leina is having trouble finding accommodations until she mentions she is in the Queen's Blade, and the greedy hotel manager rushes to fill her order and ends up rooming her with Echidna. Tomoe and Shizuka meet Melpha, and Tomoe admires her for dressing more appropriately than other competitors. It is revealed that Nyx used to be a maid for the Vance Family, and was treated cruelly by Elina. Aldra wants a new servant to lead the Assassins, and sends a fake letter to lure Risty to her palace. Once there, she awakens the hate in Risty's soul, making Risty her servant. The first match is fought: Tomoe vs Melpha, where Tomoe finds that Melpha uses lewd "Holy Poses" to fight, giving Tomoe the resolve to defeat her perversion. Another match begins: Elina vs Nyx.

It is revealed that Nyx is enslaved to a tentacle demon lord named Funikura, who has given her magical fire power, yet often molests her with its tentacles. Elina realizes that Nyx is a coward without Funikura, and tricks her into relinquishing it, upon which Nyx surrenders. Risty is revealed as the new leader of the Assassins of the Fang. Aldra turns Funikura to stone, saying that old demons should not wander free. Nowa gets lost in the Gynos marketplace and is almost raped by a gang of street punks who were swiftly beaten by Echidna. Nowa and Alleyne are summoned to fight in a swamp, as are Echidna and Irma. It is then revealed to be a team match: Alleyne and Nowa vs Echidna and Irma.

Irma refuses to help Echidna, so Alleyne and Nowa resolve to pick them off one by one. Echidna's past is revealed. Echidna manages to trap Alleyne in a pitcher plant, then to pin Nowa. Alleyne breaks free and takes the initiative against Echidna, but Irma appears, threatening to kill the trapped Nowa and forcing Alleyne to surrender. Leina brings her sword to Cattleya for repair again, while Ymir's attempts to sell weapons go unnoticed in the market. Cattleya states her resolve to reunite her family. The next set of matches begins: Reina vs Ymir and Cattleya vs Airi, the latter being fought in the room where Aldra keeps all of those she has turned to stone.

Ymir uses the fact that her bout is being broadcast to advertise the effectiveness of her weapons, especially since Leina is using a Cattleya weapon. Leina emerges victorious, however. Lana is hanging on to Cattleya during her fight with Airi, but actually proves to be helpful as Airi cannot bring herself to kill him. Cattleya is winning when she sees that Owen is frozen inside one of the stones in Aldra's "Palace of Grief" and breaks down crying, conceding defeat. Aldra promises to reunite Cattleya with her husband, and does so by turning her to stone as well. Filled with grief, Lana grabs Cattleya's spear and tries to attack Aldra. Aldra is about to turn him to stone too when Airi rescues him and they escape. They are confronted by Risty and the Assassins of the Fang, but when Risty is about to strike Lana down, she remembers the orphans she used to care for and hesitates, allowing them to escape. Lana keeps following Airi around, and she resolves to care for him in Cattleya's stead. When Cattleya does not return, Ymir asks Leina to allow her to care for her sword from now on. The next match is set: Claudette vs Menace.

Claudette and Menace are fighting in a desert, giving Menace the upper hand. Her sand attacks confuse Claudette, and she uses cursed attacks to drain Claudette's strength. It begins to rain, however, which weakens her sand attacks, and Claudette emerges victorious. Menace is later turned to stone by Aldra, who says that ancient things should stay in the past. The first round is over, with Risty advancing by some unexplained method, and Nanael advancing because her foe (presumably Melona) did not appear. Nanael is dismayed that no one is placing bets on her, and uses all of Melpha's money to place a large bet on herself while in disguise, so as Melpha's roommate, she must subsist on vegetables from her garden. Meanwhile, Risty is pursuing Irma throughout the city. She corners her and is about to kill her when Echidna intervenes and shelters Irma for a while, but Aldra sets the next match so that Irma must fight Risty anyway. Tomoe is also summoned to fight Elina.

Irma looks for an opening to strike in her fight with Risty, and finds one when Risty starts having flashbacks to her old, righteous self. However, Irma misses in her killing blow, and is defeated instead. Echidna retrieves her afterwards, and the two depart together. Elina shakes Tomoe's resolve by calling her a hypocrite in regards to how she can call herself righteous while killing people. Tomoe tells Elina she has formed a bond with Leina, since they shared food and shelter on their journey, which Elina misinterprets, thinking that Tomoe has slept with Reina. Elina attacks in a frenzy, but Tomoe pulls through victorious. Ymir is pondering how best to augment Leina's sword. The next match is set: Nanael vs Airi in the Palace of Grief. Tomoe returns from her victorious battle to find a note from Shizuka, leading her to a graveyard. Shizuka reveals that she never actually left the Kouma Ninja, and has been posing as Tomoe's friend to lower her guard so she could kill her. Tomoe finally gains the will to fight her friend, and kills her. In dying, Shizuka says that being able to kill her best friend has made Tomoe stronger since these emotional bonds would only hinder her resolve as a warrior.

Airi and Nanael are both desperate to finish the match quickly, as both are starving, and begin to fight in earnest. Airi weakens Nanael by causing her to spill more of the sacred milk, which spills onto some of the petrified people in the palace. Airi runs out of time because it has been too long since she has consumed vital force and due to her desire not to do so in front of Lana, and Airi disappears. Aldra is visibly disturbed by the spilling of the sacred milk. Lana has lost another guardian, and this time goes to Ymir, deciding to help her fix Leina's sword. Lana reveals Cattleya's fate to Ymir and Leina, and Leina says she will save Cattleya. The sacred milk causes the stone Melona was encased in to crack, and she manages to escape. Nanael is then set against Leina, but Nanael is now weak from having spilled the sacred milk, and with her new sword Leina easily defeats her. Count Vance puts a plot in motion to seize the throne for himself. Melona appears before the defeated Nanael with a proposal to defeat Aldra. The next match is set: Claudette vs. Risty.

Claudette and Risty are fighting in the courtyard of Vance Castle just as Vance's army is leaving in his bid to overthrow Aldra by conventional military force. Claudette is initially victorious, knocking out Risty with a lightning bolt. She tries to dissuade the Count from his attempted overthrow, saying that it will only breed war across the continent, and reveals that Lady Maria, Vance's wife and her adoptive mother, told her to heal Vance's pain if she did not return from the Queen's Blade, and she has been serving loyally to soothe Vance's emotional scars. Vance tries to convince her to serve him again in his bid to overthrow Aldra, but she refuses, and he tells her to leave. Risty then awakens, however, and it is now apparent that she was sent to kill the Count. Claudette manages to stop her, but is eventually defeated herself when Risty collapses a roof on her. As Claudette is teleported back to Gynos, she reconciles with the Count, who then withdraws his army. Aldra calls it a success: though the Count still lives, his coup was thwarted. Claudette warns Leina that Risty has changed. Meanwhile, it is seen that Nyx has found a job as a barmaid, and that Tomoe is training fiercely, now wearing Shizuka's old horned headband. Melona, Nanael, and Melpha discuss the mysterious Aldra, and Melona steals Nanael's sacred milk.

Nanael is drinking milk to drown her sorrows at the bar where Nyx works, and Nyx tells her of the rumor about the horned monster seen in the woods. Nanael thinks it might be Melona, and goes to seek her with Melpha. She instead finds Tomoe in a dangerous mood. Elina returns home after Claudette tells her that she is the only one of the three sisters capable of serving Count Vance any more, as neither Claudette nor Leina have the will to. Nanael tries to get Leina to ambush Tomoe in the forest, but then decides to tell her what they know about Aldra so far. Between them, Nanael, Leina, and Ymir determine that Aldra has to be allied with some sort of heavenly creature because the sacred milk actually has a negative impact on the divine (and conversely a positive one on the demonic, which is how it was able to revive Melona). Melona spies on the conversation, posing as Lana. Leina is summoned at last to fight Tomoe, and they battle in the ruins of Tomoe's old shrine in Hinomoto. Tomoe's hair has turned white, and Aldra says that she is driven by the ghosts of her friends and the suffering in her heart. Tomoe says that, for Shizuka's sake, she has become a demon who will win at any cost. A desperate fight begins with Tomoe having the upper hand, utilizing a lot of powerful techniques. Leina eventually recovers and says that she cannot lose either, and that she accepts everything that has happened, including Tomoe's feelings. Tomoe rejects that, replying that one needs to be heartless to be strong. Leina triumphs, and Tomoe claims she finally understands her. Ymir uses the fight as advertising for the sword she re-forged, and sells many cheap knockoffs of it. Tomoe awakens in the Palace of Grief.

Tomoe demands to know why Aldra had the Kouma Ninja attack Hinomoto. Aldra says that she has been searching for her sister, and Hinomoto is the only area outside of her rule. She says burning the country to the ground would be worth it to find her sister. Aldra's past is revealed: she and her sister were outcasts for being of mixed demonic descent, and were forced to wander. Her sister mysteriously disappeared one day at the edge of a forest, and Aldra, in desperation, found a spirit without a body. The spirit inhabited Aldra's body in return for giving her great power and eternal youth. Aldra offers Tomoe rule over Hinomoto in exchange for her servitude, promising peace for Hinomoto if her sister is found, but Tomoe rejects her offer, remaining loyal to her Empress. Nanael has mysteriously returned to Heaven, and Leina and Risty finally fight. Leina fends off Risty's aggressive style, and eventually causes her to hesitate when she shows her the lucky coin she gave her. Leina scores a hit and Risty falls. Leina rushes to tend to her, and Risty temporarily breaks free from Aldra's control. Aldra's evil spirit then possesses Risty directly, however, and Risty begins strangling Leina. Leina is about to pass out when Melona appears in Aldra's throne room and coils up her body, shaking her control over Risty. Leina uses the opening to break free and eventually defeats Risty, shattering Aldra's control over her for good. Melona and Aldra fight, with Melona managing to dump what remains of the sacred milk on Aldra, weakening her, but Aldra manages to drive Melona off anyway. The final battle is set to begin: Leina vs Aldra.

Nanael makes her report to Heaven, where the Head Angel determines that Aldra has made a pact with Delmora, a fallen angel. The final battle begins, with Aldra proving to have overwhelming power. She eventually kicks Leina in the neck, making her collapse. Risty appears at the arena and cheers Leina on, causing her to get back up. Leina shows that she has adopted many of her old foes' techniques as she hits Aldra with Claudette's Thunderclap Strike and Tomoe's Warrior Kick. Just as Leina has the advantage, however, Aldra petrifies her. The crowd jeers, calling her a demon. Meanwhile, Lana has invaded the palace, trying to rescue his parents by himself. He is confronted by a Fang Assassin, but finds Airi's Scythe which still contains some of Airi's spirit. He hurls the scythe at the Assassin, and Airi snags enough of the Assassin's vital force to reconstitute herself. Nanael overhears the struggle and arrives with more sacred milk, freeing Cattleya and Owen. Melona has been hiding in the palace, though now she is tiny, and Menace is also freed. Aldra flies into a rage at the crowd's jeers and petrifies them all except Claudette, Tomoe, and Risty. Even though Leina is petrified, her spirit causes everyone's weapons to glow: even those far away like Nowa and Echidna, showing the bonds she has formed with all of them. Nanael frees Leina with more sacred milk, and she counterattacks. Delmora convinces Aldra to remove the seals on his power, but even with his unsealed power, Leina defeats Aldra, causing Delmora to emerge. It is revealed that Delmora separated Aldra from her sister so that she would despair and seek to use his power for revenge so that he could get her body in return. Nyx sees that some of those petrified have been freed, and finally shows resolve of her own by freeing Funikura herself. Nanael pours more sacred milk on Delmora, then Claudette, Tomoe, and finally Leina attack, defeating him as Leina emerges victorious. Aldra matures to adulthood in an instant since Delmora had given her eternal youth, and Tomoe tells her that she can seek her sister in Hinomoto herself. Soon after, Leina is crowned the new Queen.