Initially founded in 1948 as the football section of the CSU Craiova sports organisation, it remained within the structure until 1991, when its league place was taken by FC U Craiova following privatisation. Between 1948 and 1991, the club won four championship titles and five national cups. Following a series of reorganisations and the eventual disaffiliation of FC U, the sports club re-established its football section in 2013. The current entity asserts the honours of the original Universitatea Craiova, a position recognised by several court rulings and the Liga Profesionistă de Fotbal, although they remain disputed by an also re-established FC U Craiova side.

In 2018, the club won the national cup, its first trophy following refoundation, and in 2021 secured its first supercup title. In European competitions, Craiova reached the semi-finals of the 1982–83 UEFA Cup and the quarter-finals of the 1981–82 European Cup. It was the first Romanian team to reach the semi-finals of a UEFA competition and remains the only one to have eliminated teams from each of the five major European leagues—England, France, Germany, Italy, and Spain. In the 2025–26 season, the club qualified for the league phase of a European competition for the first time, following success in the Conference League play-off round.

"The White-Blues" play their home matches at the Stadionul Ion Oblemenco, which has a capacity of 30,929. They maintain several rivalries, most notably with Dinamo București.