While the Culture is normally pacifist, Contact historically acts as its military arm in times of war, while Special Circumstances can be considered its secret service and its military intelligence. During war, most of the strategic and tactical decisions are taken by the Minds, with apparently only a small number of especially gifted humans, the "Referrers", being involved in the top-level decisions. It is shown in Consider Phlebasthat actual decisions to go to war (as opposed to purely defensive actions) are based on a vote of all Culture citizens, presumably after vigorous discussion within the whole society.

It is described in various novels that the Culture is extremely reluctant to go to war, though it may start to prepare for it long before its actual commencement. In the Idiran-Culture War (possibly one of the most hard-fought wars for the normally extremely superior Culture forces), various star systems, stellar regions and many orbital habitats were overrun by the Idirans before the Culture had converted enough of its forces to military footing. The Culture Minds had had enough foresight to evacuate almost all its affected citizens (apparently numbering in the many billions) in time before actual hostilities reached them. As shown inPlayer of Games, this is a standard Culture tactic, with its strong emphasis on protecting its citizens rather than sacrificing some of them for short-term goals.

War within the Culture is mostly fought by the Culture's sentient warships, the most powerful of these being war-converted GSVs, which are described as powerful enough to oppose whole enemy fleets. The Culture has little use for conventional ground forces (as it rarely occupies enemy territory, and has little territory of its own); combat drones equipped with knife missiles do appear in Descendant and "terror weapons" (basically intelligent, nano-form assassins) are mentioned in Look to Windward, while infantry combat suits of great power (also usable as capable combat drones when without living occupants) are used in Matter.