Lokomotiv Plovdiv is a club assembled from many parts. Its roots lie in Sportclub Plovdiv, formed in July 1926 when two district teams, Karadzha and Atletik, merged and chose white, black and red as their colours, which the club still wears. A second root is ZSK Plovdiv, founded in 1935 as the sports club of the railway workers. After 1944 the Communist authorities reorganised Bulgarian sport on the Soviet model, and Sportclub was merged with Armenian and Catholic district clubs, then with the cooperative team Petar Chengelov. It passed through the names Slavia and Torpedo, and merged with the railway club in 1951. The name Lokomotiv Plovdiv has been used since then and was settled in its present form in 1957. The supporters followed the colours and the players through every change, and this continuity is the real identity of the club, whose nicknames are The Black-Whites, The Railwaymen and The Smurfs.
The first great European night came in 1964–65. In the Inter-Cities Fairs Cup, Lokomotiv eliminated Vojvodina and Petrolul Ploiești and reached the third round against Juventus. Both legs ended 1–1, and a play-off in Turin was lost 1–2. The home leg drew a record European crowd of 40,000. The leading figure of that era was Hristo Bonev, who holds the club records for league appearances (404) and league goals (180), and who later led Lokomotiv to the Cup of the Soviet Army in 1983, a 3–1 win over Chirpan that the Bulgarian federation does not count as a Bulgarian Cup. The club had won silver medals in 1973 and bronze in 1974, and since 6 September 1982 it has played at the Lokomotiv Stadium, known as Lauta after the park in which it stands.
The only league title came in 2003–04. The club had been bought in 2001 by Georgi Iliev, who merged it with Velbazhd Kyustendil, and under the coach Eduard Eranosyan the team led by six points at the halfway stage and finished with 75 points, three more than Levski Sofia. The title was secured in the penultimate round with a 3–2 win over Slavia Sofia in front of more than 17,000 spectators, and Martin Kamburov was the league's top scorer with 25 goals. About 50,000 people gathered in the city's main square to celebrate. On 31 July 2004 captain Ivan Paskov added the Bulgarian Supercup with a header in the last seconds against Litex Lovech. The Champions League qualifier against Club Brugge, lost 0–4 and 0–2, was a sobering start in Europe, and in 2005–06 the UEFA Cup run ended against Bolton Wanderers, who won 2–1 in both legs.
The second golden period followed under the coach Bruno Akrapović between 2017 and 2020. On 15 May 2019 Lokomotiv won its first Bulgarian Cup by beating local rivals Botev 1–0 in Sofia, with Alen Ožbolt scoring in the 72nd minute. On 1 July 2020 it retained the trophy by beating CSKA Sofia on penalties (5–3), the first back-to-back winner since Litex in 2008 and 2009, and on 2 August 2020 captain Dimitar Iliev won the Supercup with a last-minute volley at Ludogorets. The European record of that period included an away-goals win over Spartak Trnava in 2019, a defeat by Strasbourg and, in 2020, a 1–2 loss to Tottenham Hotspur coached by José Mourinho, in which two red cards turned a lead at one point to a defeat. In the same year it finished second in the league with 61 points, its second silver medal, and in 2021 it reached the third qualifying round of the Conference League, where Copenhagen won 5–3 on aggregate.
The club's rivalries define its calendar. The Plovdiv derby against Botev is regarded as the second fiercest in Bulgaria after the Eternal derby, and matches with CSKA Sofia carry the old rivalry of the two cities. Its supporters have a long friendship with fans of Napoli. In 2025–26 the club finished fifth in the First League, and it remains one of the best supported teams in the country.