They have played at the DW Stadium since 1999, which they now own, sharing the stadium with rugby league club Wigan Warriors. They previously played at Springfield Park for 67 years.

As of the 2009–10 season, Wigan Athletic are the youngest club in the Premier League, having only been formed in 1932.

Wigan Athletic FC was formed in 1932, following the winding up of Wigan Borough the previous year. Wigan Athletic was the fifth attempt to create a stable football club in the town following the demise of Wigan County, Wigan United, Wigan Town and Wigan Borough. Springfield Park, the former home of Wigan Borough, was purchased by the club and they were elected to the Cheshire County League.

In its early history, Wigan Athletic's most notable exploits came in the FA Cup. In the 1934–35 season, Wigan Athletic beat Carlisle United 6–1 in the first round, setting a cup record for the biggest victory by a non-league club over a league club, a record only equalled in 1955 by Boston United, and again in 1957 by Hereford United.

In 1945, Wigan Athletic were elected to a different league, the Lancashire Combination, and in 1950 came close to election to the Football League, narrowly losing out to Scunthorpe United. In the 1953–54 season, Wigan Athletic played an FA Cup match against Hereford United in front of a crowd of 27,526, a Wigan Athletic record and also a record for a match between two non-league teams at a non-league ground. In 1961, the club moved back to the Cheshire County League.

In 1968, Wigan Athletic were founder members of the Northern Premier League, known since 1994 as the UniBond League. Winning the league title in 1970/71, Leading goalscorer with 42 goals, including 7 hatricks, was Geoff Davies who scored 28 goals in the following 1971/72 season. He left to play in America with Eusebio, (and against Pele, George Best, Rodney Marsh, and Franz Beckenbauer). After 34 failed election attempts, including one controversial but headline-making application in 1972 to join the Scottish League Second Division, Wigan Athletic were elected to the Football League in 1978.

The first floodlit match was played at Springfield Park on 19 October 1966, when Wigan Athletic played Crewe Alexandra, with the official opening of the floodlights on 24 October 1966, when Manchester City were the visitors. City brought a full strength team to Springfield Park and won 4–0.

Wigan Athletic finished in second place in the Northern Premier League in the 1977/78 season, behind winners Boston United. But as Boston's ground and facilities did not meet the Football League criteria for a League club, whereas Springfield Park did, Wigan Athletic were put forward for election to the league. There was no automatic promotion to the Football League until 1987, and at that time a club had to be 'voted out' of the League to allow a non-league team to be promoted in their place. At the end of the 1977/78 season, Southport finished next to bottom of the old Fourth Division, and faced off with Wigan Athletic for their place in the League. The first round of voting was tied, with both clubs receiving 26 votes. After a tense re-vote which Wigan controversially won 29–20, Southport lost their place in the Fourth Division and Wigan Athletic became an English League club on 2 June 1978.

In the club's first season of League football, Wigan Athletic finished in sixth place, just six points off promotion and playing in front of an average crowd of 6,701. Two more top-half finishes came in the following seasons. They gained their first Football League promotion under the management of former Liverpool player Larry Lloyd in 1981/82, when a points tally of 91 saw them join the former Division Three for the first time, beginning a 10 year spell in English football's third tier. The club struggled in their first season in Division Three, which led to Lloyd's controversial sacking in early 1983, being replaced by Harry McNally. Under McNally's management, the club stabilised in Division Three and secured a pair of mid-table finishes, but a dreadful 1984/85 season cost him his job, with Tranmere manager Bryan Hamilton stepping into the breach. Under Hamilton's management, the club's performances went to the next level and they won their first silverware as a League club that season with the Freight Rover Trophy. They were beaten in the Northern Final of the same competition the following season by Bolton Wanderers. More importantly, Hamilton achieved Division Three survival, which had looked an impossible task earlier that season.

The 1985/86 season saw a marked improvement in the club's league form, eventually finishing in fourth position, a then-club record high which would stand for 17 years until 2002/03. Wigan finished the season just one point outside the promotion places in the final season before the Football League introduced the play-off system for promotion and relegation. However, Hamilton's feats attracted the attention of First Division Leicester City and he left to become their manager in the summer 1986. His assistant, Ray Mathias, who had followed him from Tranmere, stepped up to the Wigan manager's job. Wigan managed an identical fourth place finish in the 1986/87 season, but this time were rewarded with the chance to compete for the final promotion place in the new play-off system. (In the first two years of the play-off system, teams finishing 3rd, 4th and 5th joined the team finishing 20th in the division above to play off for the promotion place; this was changed to the teams finishing 3rd, 4th, 5th and 6th from the 1988/89 season). The Latics lost at the two-legged semi-final stage to Swindon, who went on to win the final promotion place.