Red vs. Blue centers on the Red and Blue Teams, two groups of soldiers engaged in a civil war. Each team occupies a small base in a box canyon known as Blood Gulch. According to Simmons (Gustavo Sorola), one of the Red Team soldiers, each team's base exists only in response to the other team's base. Although both teams generally dislike each other and have standing orders to defeat their opponents and capture their flag, neither team's soldiers are usually motivated to fight each other- if they are otherwise, neither are efficient. Teammates have an array of eccentric personalities and often create more problems for each other than for their enemies.
Grif is still despairing over being back in Blood Gulch, despite the others' attempts to shut him up. Meanwhile, back at Zanzibar, Tex, Tucker, and Caboose discover that Church is back in ghost form again. Church explains that he was literally scared out of his body after being ambushed by the Alien in the last episode, though his attempts to explain this are repeatedly interrupted by Caboose's stupidity and Tucker's attempt to hijack the flashback and showcase his sexual fantasies; Tucker wisely ends quickly so as to avoid getting his head blown off by Tex. Tucker uses the catch phrase "Bow-chicka-bow-wow" in this episode for the first time, much to Church's annoyance.
In Blood Gulch, the Red Team takes potshots at Grif with their sniper rifles in order to get him to stop screaming. Grif eventually relents, and the team prepares to investigate their old base. Sarge gives a speech about alertness, completely unaware that Sheila is roaming around behind him. Meanwhile, the Blues prepare to hunt the Alien that scared Church. When asked about the Alien's whereabouts, Andy proves unhelpful, merely offering insults instead. Suddenly, the Blues spot the Alien, causing them to fire wildly and run away in panic - with the exception of Caboose, who simply asks, "Did we win?". The episode ends with Andy laughing and mocking the sudden retreat.
Simmons tries to convince Sarge that he did see a tank behind him. Donut concurs, but Sarge disregards his testimony because he is "impressionable", and Grif simply denies it in order to make Simmons look bad. Meanwhile, the Blues insult each other over their previous panicked, wild fire attack on the alien. Tex decides to go in alone and dashes into the complex while the rest debate Church's heroism (or lack thereof). Upon entering the complex, Tex is immediately cut down and re-appears in ghost form. Back at Blood Gulch, Simmons and Donut get into a fistfight/hijacking match over the hovercraft, which Simmons wants to use to find the tank. Believing that Simmons has gone insane, Sarge promotes Grif to his "Number Two" man, but Grif quickly loses the position due to his laziness. On the Blue side, Tucker suggests that Caboose goes into the complex and speak to the alien. Church likes the idea because he and Tex could sneak in and retrieve their bodies while the Alien is chewing on Caboose. Caboose enters, sees Andy, and asks whether he has seen the Alien. As he finishes his sentence he sees the Alien's shadow on the ground.
Simmons has completely fallen out of favor with Sarge, and in fact is now ordered by the judge — Donut wearing a judge's wig — to stand at least 200 yards away from the rest of the Reds. As a result, Sarge begins to hold a competition to determine who will be his new right-hand man. Grif is automatically disqualified for being Grif, which puts the competition down to Donut, Lopez's old wrench, and a skull found nearby. Simmons laments the ruination of his life, and concedes to himself that maybe he did imagine seeing the tank. Sheila's voice is suddenly heard right behind him, begging to differ. Meanwhile, back at Zanzibar, the Blues are startled to discover that Caboose has actually managed to tame the Alien, thanks to his kindness — or, more likely, that the alien found him unpalatable, and no longer wants to eat him or anything that looks like him. The Blues insult the alien while trying to understand its language, which seems to consist entirely of blarg and honk.
At the Zanzibar fortress, Church asks Gary whether he can translate the Alien's speech for them. Gary reveals the alien's race were his creators, but unfortunately he knows virtually nothing about the race because he was programmed entirely with knowledge of the Shisno. The Blues continue to try translating what the alien is saying, and eventually reach the conclusion that the Alien's name might be "Honk Honk". Church even believes that he figured out that blarg means yes in the alien's language, though Tex argues that it could also mean no. Meanwhile at Blood Gulch, the Reds continue Sarge's right-hand-man contest, which Donut ultimately wins. Simmons has become despondent and suicidal, and Sheila (whom Simmons believes is a figment of his imagination) tries to cheer him up by leading him back to her home, a reconstructed Blue base. Sheila reveals that she has lost many of her memories due to circuit degradation over the years. She knows that her final mission was to protect the Blue Base from the enemy of the Blues, and though she has forgotten their identity, she vaguely remembers it was an army of a different color. Simmons, immediately realizing that his life is in danger, unsuccessfully tries to convince Sheila that the enemy was space pirate cowboy monkey ninjas who were trying to round up some cattle.
The episode opens up again at the Zanzibar fortress as Tucker and Caboose are attempting to teach English to the Alien. Church and Tucker get into a small debate on whether they should teach the alien English or learn his language. Tucker is convinced that they should teach English to the Alien and even had created some visual aids. As it turns out, Tucker was able to get the writing supplies from Caboose's gun which apparently contained crayons instead of bullets. However, when Tucker activates his energy sword to cut the poster boards, the Alien jumps over and attacks him. Despite Tucker's cries for help, Church watches the Alien as it attacks Tucker in order to "evaluate" his fighting style.
Back at Blood Gulch, Simmons is at the Blue base with Sheila close by. He attempts to contact the Red Base, but is greeted with Donut on the line, who tries to impersonate an answering machine. Simmons attempts to get Sarge on the line, but Donut, under instructions from an off-screen Sarge, denies Simmons from communicating with Sarge, even after he informed Donut that he had captured the Blue Base and Sheila. Eventually Donut hangs up on Simmons, but not before letting Simmons know that he really enjoys his new job as Sarge's right-hand man. Simmons then declares that he will kill all the Reds and tells Sheila to "lock and load".
Back at Zanzibar, Tex talks with Andy. Tex, through some bluffing and mild threats of blowing up Andy with a remote detonator, convinces him to help her translate what the alien is saying. This, however, doesn't stop Andy from making rude jokes about Tex acting more male than female.
At Zanzibar, Tex and Church argue over whether to let Andy translate what the Alien is saying. Church is concerned that Andy's lack of manners could upset the alien even further. Eventually, Church relents and agrees to this arrangement out of his curiosity as to what could happen. During this whole conversation the Alien is still beating Tucker to a pulp.
At Blood Gulch, the Reds are fracturing even more as Donut is unsuccessful in asking Grif to return to their base. Grif refuses, believing Sarge simply wants him to do work, and not just eat ice cream. In reality, Sarge did want Grif to help him eat some of the ice cream that he found. Simmons — now painted mostly blue — plays out his vengeance on the Reds. At first he attempts to cause the Reds to be jealous of him; he soon gives up and orders Sheila to attack the Red base.
At Zanzibar, with Andy acting as a translator, the Alien reveals that he came to retrieve the energy sword that Tucker found. It was part of the sacred quest that he was on, but the sword has now locked itself to Tucker as he was the first to find and use it; this explains why Tex was unable to use the sword. As a result, Tucker must join the Alien on its quest. If Tucker refuses, the alien will destroy the base and slaughter everyone in it.
On Zanzibar's beach, Tucker finds himself as an involuntary sword-bearer as he is forced to partake of the sacred quest that has some resemblance to The Lord of the Rings. After the Alien explains the lands that he and Tucker will travel through, Church informs Tucker (the fighter) that Caboose (the wizard), Andy (the archer), and the alien (the healer) will be the team that goes out on this quest. Though this quest is pretty much a suicide mission, Tucker does warn Church that he better hope that Tucker survives, or he will be forced to take care of any children that Tucker might have.
At Blood Gulch, Simmons' attack on the Red Base continues. However, he has been so indoctrinated with hatred of the Blues that all of his insults and attack orders confuse the words Red and Blue. Grif, still watching Simmons and Sheila fire upon the Red Base, convinces Simmons to come back to the Red Base. Despite the selfishness of Grif's reasons, Simmons admits he misses the old days. However, just as he is about to go back to the Reds, Sarge sees that Simmons has painted his armor mostly blue and is unable to accept him back. Sarge says he can understand many things, even the reasons for attacking one's own base out of anger, but to see one of his former soldiers wear the colors of the Blues, is unacceptable.
On the beach of Zanzibar, Church tries to give some last-minute advice and parting words to Tucker and the rest of the quest-team before they begin their trip. Tex apparently has a strong attraction to masculine objects, whether it was Tucker's energy sword, or the Alien's rather muscular naked body, or specifically one part of it. Church attempts to say some encouraging words to Tucker, but this fails as Tucker frustrates Church's attempts. As the team leaves, Church remarks to Tex that he is surprised that she did not go with the rest of the group as quests usually have a goal of riches or power at the end of them. As he finishes his sentence, he assumes correctly that Tex has left.
Back at Blood Gulch, Simmons decides to take Grif back to the blue base as a hostage. After some prodding from Grif about not being "properly treated" as a hostage — in other words, Simmons wasn't being mean to him — Simmons starts hitting him. Simmons pushes Grif into what he thought was a hole, but it turns out to be part of a gravity lift that keeps putting Grif behind Simmons. The episode ends with Simmons getting frustrated each time he pushes Grif into the hole.
Having arrived at the Great Burning Plains (Burial Mounds), the Sacred Quest team prepares to perform one of the many tasks that the hero of the Alien's prophecy is supposed to do. As the team argues and bickers, it is revealed by the Alien and Andy that they know what Earth is, and that they don't have a favorable opinion about the planet. Apparently, the Alien's race invented the telephone a thousand years before humans did, which, however, fails to impress Tucker, due to the limited verbal communication of the alien race. In the meantime, Caboose scouts ahead and claims to recognize the area.
The Alien warns the group that they are about to encounter a monster, which they have to conquer by distracting it and hitting it's weak spot. Tucker is unmotivated about the plan, even to the extent of having paid no attention to the details of the monster's weak spot. After they finally leap down the last ridge, they see the skull of the monster, which Tucker realizes is that of a cow, with a broken skull as the only visible remains, possibly due to one of the Red and Blue Teams' scavenging missions in season 3 (episodes 43–46); Caboose confirms to Andy and the Alien that they had been there before.
Back at Blood Gulch, Sarge assumes that Grif is being tortured by Simmons, a concept he's very satisfied with. Donut, however, in his current status as manager, breaks the harmony by proposing bureaucratic changes. Sarge decides that he can't take this anymore, but is reluctant to rescue Grif - a situation he just can't find the name for, but finally settles with conundrum.
Sarge and Donut enter the Blue Base to rescue Grif without encountering any perimeter defense, such as Sheila. Inside the base, Grif is still playing with the gravity lift that Simmons originally mistook for a hole. As Grif runs to and fro on it, both Simmons and he question how Sheila was able to upgrade the base without any tools or arms. Simmons then concludes that if he could somehow determine the real truth, he could reconcile with Sarge. At this point, Sarge intervenes, knocking Grif out. Before Sarge can execute Simmons for treason, however, Church appears and knocks Sarge out from behind. Church mistakes the mostly blue Simmons as a Blue soldier native to the future.
The Sacred Quest team finds itself in a swamp (Backwash), where Andy says they can rest and sleep for a while. However, with strong allusions to The Lord of the Rings, Caboose notices that something has been following them. Andy confirms that this Gollum-like creature has been following them since the beginning of their journey. Later that night, Tucker awakes to find that he is apparently alone in the swamp. As he begins to look for his companions, the mysterious figure approaches Tucker from behind (as he is being used as bait). The Alien ambushes the intruder, who turns out to be Tex. She then joins the team after being promised the sword upon completion of the quest.
In the basement of the Blue Base in Blood Gulch, Simmons covertly talks to Donut about keeping his true identity hidden from Church. Donut, however, does not actually recognize Simmons. Church soon appears after dropping Sarge's body into the basement, and the three proceed to load Sarge and Grif into the jeep.
Meanwhile, the Sacred Quest team reaches the edge of the Great Freezing Plains (Containment) that the Alien had mentioned. This particular part of the quest requires that the hero gain access to the temple ahead, which is heavily guarded by a large number of guards. With this information, Tucker wants to retrace their steps to recover a mitten that Caboose lost, but Tex takes the initiative and decides to attack the temple guards under the protection of her cloaking device.
Back at Blood Gulch, Church and Simmons drop off Donut and the still-unconscious Sarge and Grif outside the Red Base. Church suggests to Donut that he lie to Sarge and Grif when they wake up, making them think he rescued them. Donut asks what Church wants, based on the precedent set by the Blues' surrender in 22. Church, considering the Reds' failed rescue mission not so much a surrender as a "total ass-kicking", decides to keep the Reds' jeep, causing Donut much despair. As Sarge begins to recover, the episode ends with Simmons knocking him out again in order to protect the secrecy of his identity.
Back at the Freezing Plains, Tex attempts her covert attack inside the temple guarded by the Red and Blue Grunts who first appeared at Battle Creek. Sneaking up behind a blue Grunt, she attempts to knock him out, without much success. Although she has to spend time beating and shooting him, the others pay no attention to his exclamations of pain and complaint. It is only when Tucker yells in reaction to their aloofness that they begin to fire. Now under attack, the rest of Sacred Quest team runs for cover while Tex kills the remaining soldiers in the temple.
In Blood Gulch, Donut, apparently having taken Church's advice to lie and portray himself as a hero, is finishing his debriefing with Sarge and Grif. While the Reds discuss and mock Donut's contrived story, Church briefs Simmons on each Red Team soldier, finishing with a critical opinion of Simmons. His ego thus wounded, the latter runs back to Blue Base to cry. Once out of Simmons' earshot, Sheila asks Church whether he realizes that he had been talking to Simmons. Church confirms that he does.
In Blood Gulch, Church relishes the fact that the Blue Team now possesses all three vehicles within the canyon. Sheila, however, is unhappy and begins to show signs of jealousy and annoyance — this portion was moved to the Deleted Scenes section of the DVD.
Back at the Freezing Plains, Andy frantically orders Tucker to open gates of the temple by using his sword as the key. The doors open, revealing an alien ship. The Alien rushes towards the ship, dropping Andy in the snow. Tex and Tucker become agitated, as the Alien had never disclosed — not even to Andy — that the quest would involve a ship, which Tex demands as her reward, nor that the sword would be used as a key. After taking off in the ship, the Alien appears to make dive attack on the other Quest members; at the last moment it is shown he was firing at a Grunt sneaking up on them. However, the Alien's ultimate intentions are left ambiguous, as Wyoming suddenly guns the ship down. As Tex leaves to pursue Wyoming for destroying her reward (the events of which are portrayed in the miniseries Red vs. Blue: Out of Mind), the Battle Creek soldiers begin to respawn, convincing Tucker and Caboose to leave.
Back in Blood Gulch, Church orders Simmons to wash the Reds' jeep, the latter, unaware that his identity is known, challenges Church's authority. In response, Church tries to demonstrate that he had led the Blood Gulch Blue Team 800 years in the past and, in the process, unexpectedly makes contact with a descendant of Vic. This descendant, who calls himself Vic Jr., scoffs at the idea of "Blue Command", leaving Church confused and wondering the outcome of the Red and Blue civil war.
In the Red Base, Sarge attempts to bury his disgust and hatred toward Grif in an attempt to consolidate whatever soldiers the Reds have left to fight the war with the Blues. Sarge's own personal disdain for Grif still leaks through as he disclosed that he has attempted to murder Grif countless times while everyone was asleep. Outside of the base, Simmons — still mostly blue — and Donut have a verbal fight. Donut, still under the impression that Simmons is a Blue soldier, refused to allow Simmons to pass without being shot at. Eventually, Sarge and Grif come out to see what's happening and acknolwedge who Simmons really is. Simmons, though still looked down upon by Sarge for his apparent betrayal, still wants to pass along Blue Army info to the Reds.
Caboose, Tucker and Andy return to the Blue Base. According to Tucker, Tex is still pursuing Wyoming, the quest was a failure, and the Alien died. Frustrated that the quest failed and that Tucker did not immediately reveal that Wyoming is still alive, Church orders Tucker to report those kind of events immediately in future.
At the Blue Base, Tucker becomes ill. Church and Caboose discuss Tucker's sickness, which apparently he caught when the Sacred Quest team stayed overnight in a swamp. Church suggests the sword's power source could be giving off radiation. Church and Caboose have a reasonably light and friendly discussion regarding the nature of the sword, as Tucker rolls in pain. This friendly discussion even extends to Church mentioning that he would love to "live in [Caboose's] world for about 10 minutes" just to have some fun.
At the Red Base, Simmons persists in trying to enter the Red Base to relay vital information about the war to the Reds. However, he still meets resistance from Donut and Grif until he very quickly changes out of his mostly blue armor to his original maroon armor. Apparently Simmons learned this ability because of his extreme shyness, which has led him to never use the base's toilet for three years.
Back at the Blue Base, Church and Caboose question Andy on what might be causing Tucker's sickness and suggest that he, being a machine (and thus not able to get sick) go into the base, find out what is wrong with Tucker and report back. Since Andy is a bomb, the only solution he can provide is to blow up the base with Tucker inside, killing all the germs and everything around the base in the process. Finally, out of frustration, he tells Church and Caboose that if they want a medical diagnosis, they need to find a doctor. With that, Caboose says to Church "Please don't do it."
O'Malley and Lopez bicker over who should pick up the telephone that is ringing inside their secret lair, while Doc decries their bickering. It appears that all three have survived their encounter with the Alien and that O'Malley has continued in his pursuit of taking over the universe. It would seem from Lopez's attitude toward O'Malley, all those attempts have failed miserably and this has caused Lopez to become quite cynical and disrespectful toward O'Malley.
Simmons manages to enter the Red Base by correctly guessing the weak password established by Grif and Donut. Simmons wants to report the Blues' plans, but Sarge still considers him a traitor and insists on holding a trial with himself as both judge and prosecutor. This trial is quickly aborted, however, when Grif argues that Donut will want to act as a bailiff in hotpants. As a result, Simmons' sentence is summarily commuted to the payment of a hefty fine, to be split between Sarge and Grif.
Meanwhile, O'Malley, Doc and Lopez return to the gulch. As O'Malley approaches the Blue Base, he is greeted with a "warning shot" from Church, who reveals to Caboose that he was actually trying to hit O'Malley. O'Malley accuses the Blues of attempting an ambush, but Church explains that he just wants to establish a few ground rules at the outset: O'Malley is supposed to enter the base, give a diagnosis for Tucker, and then leave. In exchange, O'Malley demands something "mysterious", "frightening", and "pure evil", as well as a 20-dollar upfront copayment. Church agrees and asks Caboose for 30 dollars.
The episode begins with Sarge, Simmons, and Grif racing toward the Blue Base. Sarge worries that, since the Blues have re-established contact with their Command, they may be receiving new intelligence, weaponry, and soldiers to aid in their efforts for the war. Grif, however, suggests that the Blue Command could simply be giving the same "generic" instructions that Red Command has been giving the Reds. Eventually the discussion changes gears and the Reds ponder where Donut could be. Simmons spots him standing next to a rock, talking to something. After taking a look through his sniper rifle, Grif sees that Donut is talking with Lopez.
Back at Blue Base, Church introduces O'Malley and Doc to Andy. An awkward moment for O'Malley occurs when Church notes that Andy had originally been designed to kill O'Malley. Andy feigns an explosion, frightening O'Malley. Church and Andy share a good laugh, while O'Malley is unamused.
Meanwhile, the rest of the Reds gather around Donut and Lopez. Donut reveals that he had taken four years of Spanish in high school, but, from the subtitles provided, he can neither speak it or understand it fluently. Eventually, after Donut fails to communicate Sarge's request to Lopez, Sarge gains root access into Lopez to force him to play back the message from Red Command stored in his memory. Unfortunately, the message, which actually contains the generic instructions that Grif had mentioned previously, is played back in Spanish. The Reds are at a loss on how to translate the message until Simmons mentions that the Blues had a bomb that could translate the message. Although Grif discourages the idea when he reminds them the bomb can explode via remote detonation as the entire team huddles around it, Sarge wants to retrieve it.
While Doc examines Tucker inside the Blue Base, the Reds digress into a discussion on the relative appropriateness of hand to hand combat, sniping, and nuclear warfare. Eventually, Sarge, with Lopez's head in tow, heads out to steal Andy from the Blues.
Doc returns outside to give Church and Caboose his diagnosis of Tucker. After prolonging his explanation of Tucker's condition for dramatic effect, he discloses that he believes Tucker is pregnant, based on the presence of two different heartbeats. Incredulous, Church goes with Doc to confirm the diagnosis, leaving Caboose alone with Andy.
When Caboose has his back turned, Sarge surreptitiously swaps Lopez's head for Andy, leaving Caboose under the impression that Andy had become a "real boy". Shortly realizing that Andy is useless without Lopez, Sarge returns, distracts Caboose, and swaps Lopez's head for a skull. Upon seeing the skull, Caboose believes that Andy has died and, in hysteria, delivers an extended soliloquy lamenting the loss of Andy.
The last episode of season 4 begins as Doc tries to convince an incredulous Church of Tucker's pregnancy. When Doc discloses the truth to Tucker, he does not believe him either, thinking he himself has impregnated someone and invents excuses. Caboose enters the base with the skull, asking for help, proclaiming that Andy is dead. After Caboose explains how he found the skull, Church decides to leave the base.
Meanwhile, Andy plays back the message from Command in English for the Reds. After hearing the generic instructions, Sarge becomes depressed, and while Grif tries to cheer him up, Donut spots Church approaching with Sheila. Sheila then fires, frightening the Red Team, which regroups behind a rock formation. Sarge calls for reinforcements, and Simmons attempts to negotiate a surrender from the Blues. Annoyed, Church explains what has just occurred back at his base. To Church's dismay, Andy lets slip that it is possible for Tucker to be pregnant, as the Alien's race propagates by infecting other lifeforms with parasitic embryos. Caboose then calls Church to inform him that O'Malley has moved to another host as the Reds had been using their radios, and that Tucker had his baby. Higher-pitched Alien speech can be heard off-screen. Church returns to Blue Base, and Donut follows him, wanting to see the baby. Sarge stops him, and orders him to wait for the ship being sent by Command. Donut argues that it could be weeks, even months before the ship arrives. A ship then promptly lands on top of Donut.