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On the world of Origin, the Flowers built a single City. The City consisted of the civilian Garden, and the Works which would eventually become the core of Headquarters. The Firstborn were primarily concentrated in the Works, and the two factions were somewhat dismissive or disparaging of each other.
As the occupants of the Works continued their research into plotholes, they eventually discovered a way off-world. The Organisation they founded in the wake of this event continued to expand its HQ, and eventually discovered how to create plotholes.
The Civil War grew out of the tension between the Organisation and the Garden. The purported cause was the Garden's continuing concern over the Organisation's plothole sustaining and creating technology; this led to the Garden government attempting to seize HQ and break up the Organisation. The Sub Rosa and Captain Dandy had prepared for the outbreak of war; they activated Case Grey, setting the Weeds in motion to defend Headquarters.
During the early stages of the war, the government managed to occupy Old HQ - the portion of Headquarters set on Origin. There were only three portals from Old HQ to the rest of the complex; when the government used fire to clear the way through one of these, the Organisation responded by breaching the glass ceiling of the First Room to which the portal led, denying the government forces entrance.
The war resulted in the formation of the Department of Intelligence from the Admin Department, creating a fourth department in the Organisation. Both sides engaged in morally questionable attacks - the government slaughtered civilians in the Admin Annexe, while the Organisation bombed the Garden - and the Organisation was ultimately defeated. Fleeing Origin, they closed all three portals back; since they were unable to create new plotholes outside of Word Worlds, no return was possible.
The Sunflower Official restructured the Organisation, giving it a new purpose and a new identity as the Protectors of the Plot Continuum. The Garden government continued to rule over Origin, and the tensions that had led to war would erupt once more in the Fall of Origin.