The club was founded in 1883, and played its matches at Feethams. The club originally played in regionally organised leagues, and were one of the founding members of the Northern League in 1889. They were first admitted to the Football League when the Third Division North was formed in 1921. They won the Third Division North title in 1925, and their 15th place in the Second Division in 1926 remains their highest ever league finish. After their admission to the League, they spent most of their history in the bottom tier. They won the Third Division North Cup in 1934, their first victory in nationally organised cup competition. They reached the last 16 of the FA Cup twice, and the quarter-final of the Football League Cup once, in 1968. In the early 1990s they won successive titles, in the Conference National in 1990 and the Fourth Division in 1991. In 2011 they won the FA Trophy, defeating Mansfield Town 1–0 at Wembley Stadium.
Darlington moved to the all-seater, 25,000-capacity Darlington Arena in 2003. The cost of the stadium was a major factor in driving the club into administration in 2012. Because the club was unable to agree a Creditors Voluntary Agreement (CVA) it was expelled from The Football Association. A new club was immediately formed but The Football Association ruled that, as a new club, it must have a different playing name from the expelled club. The name chosen was Darlington 1883, and that club was placed in the Northern League Division One, the ninth tier of English football, for the 2012–13 season. They won three promotions in four seasons before the FA approved their request to change to the traditional Darlington FC name.
The club's traditional colours are black and white shirts, black shorts and black and white socks. The club's crest depicts Locomotion No 1, referring to the town's railway history; as well as a stylised Quaker hat, referring to the religious movement that had a historic influence on the town, and which was the source of the team's nickname, the Quakers.
The club's main rivals historically has been Hartlepool United.
In July 1883, a meeting was called in Darlington Grammar School to address concerns that so few Darlington-based football clubs were entering the major competition in the region, the Durham Challenge Cup. The meeting agreed with the view expressed by the Darlington & Stockton Times newspaper, that there was "no club, urban or rural, sufficiently powerful to worthily represent Darlington", decided to form a new club, and elected one Charles Samuel Craven, a local engineer, as secretary. Darlington Football Club duly entered the Durham Challenge Cup, reached the final in their first season, and won the trophy in 1885. The following season Darlington entered the FA Cup for the first time, only to lose 8–0 to Grimsby Town. Craven was instrumental in the formation of the Northern League in 1889. Darlington were one of the founder members, and went on to win the league title in 1896 and 1900; they reached the semi-final of the FA Amateur Cup in the same two seasons.