The club first appeared in 1977 and in their debut season in the Latvian league finished 7th out of 13 teams. After three less than stellar seasons the club changed owners – it was attached again to the bus factory and renamed to Automobīlists Jelgava.
As Automobīlists the Jelgava squad also had it hard – at best it finished seasons in the middle of the table, and between 1983 and 1987 it played in the 1st league. In 1987 Automobīlists lost to Zemgale Ilūkste for a place in Virslīga but as the league was expanded under the name of RAF, Jelgava once again had a club in the top Latvian league.
In 1988 and 1989 there were two teams of RAF Jelgava which in 1990 merged into one. One of those played in the lower Soviet leagues, the other – in the Latvian league. In 1988 and 1989 under the management of Viktors Ņesterenko the "local" RAF won the Latvian league, in 1988 as a golden double it also won the Latvian Cup. Meanwhile the "international" RAF weren't doing that well – although they had in its squad several talented young players including Vladimirs Babičevs, Dzintars Sproģis, Igors Troickis and Aleksandrs Stradiņš, its results were very disappointing. In 1989 Ņesterenko took over the unified RAF team in the Soviet league and in the Baltic league. In 1990 and 1991 the team played better, but then the Soviet Union collapsed and RAF joined the Latvian Virslīga.
In the early 1990s RAF was one of the strongest teams in Virslīga, three times finishing second and once third (in 1992 they finished runners up to Skonto Rīga in an additional game after finishing the season on equal points). However, when the plant ran into financial difficulties, the team received new sponsorship from the University of Latvia in 1996 and, as a result, changed their name and relocated to Riga, and played in the Latvian University Stadium. 
As RAF Rīga the club only played one season, finishing 5th in the Latvian league, however it won the 1996 Latvian Cup. But after the season the club changed its name again – this time to Universitāte Rīga.
In the 2010 season Jelgava was the only Latvian football club which won a game in European football tournaments (2:1 against Molde).
On 2 September 2010 FK Jelgava played a friendly against Premier League club Blackpool. The match marked the opening of the Olympic Sports Center of Zemgale. The President of Latvia Valdis Zatlers and the British Ambassador in Latvia attended the game.