Professional football (and professional sport in general) developed more slowly in Southern England than in Northern England. Professionalism was sanctioned by The Football Association as early as 1885, but when The Football League was founded in 1888 it was based entirely in the north and midlands with the County Football Associations in the South being firmly opposed to professionalism.
Woolwich Arsenal (nowadays simply Arsenal) were the first club in London to turn professional in 1891 and were one of the prime motivators behind an attempt to set up a Southern League to mirror the existing Northern and Midlands based Football League. However, this venture failed in the face of opposition from the London Football Association and Woolwich Arsenal instead joined the Football League as its only representative south of Birmingham in 1893. Additionally, an amateur league, the Southern Alliance was founded in 1892, with seven teams from the region, but that folded after one incomplete season.
Nonetheless, another attempt was made to form the Southern League, and this time it was successful. A competition for both professional and amateur clubs was founded in 1894 under the initiative of Millwall Athletic (now simply Millwall). Initially only one division was envisaged, but such was the enthusiasm, that eventually two divisions were formed
The Southern League soon became the dominant competition below The Football League in Southern and Central England. By the turn of the century a few of the Southern League sides began to rival the Football League in the FA Cup but overall it was still regarded as the equivalent to the third level of English.
Two Southern League clubs, Southampton (in 1900 and 1902) and Tottenham Hotspur (in 1901) reached the final of the FA Cup around the turn of the century. Tottenham Hotspur are the only club from below the 2nd level of English football to have won the FA Cup.
Several of the best players in England moved from the Football League to the Southern League around this time, due to the restrictions on their freedom of movement and wages implemented by the Football League between 1893 and 1901, and the failed efforts of the Association Footballers' Union (the AFU) to relax the restrictions.
The champions of the two leagues during this period met in the annual Charity Shield. Out of the six meetings the respective league champions had in the Shield, however, only one was won by the Southern League champions – Brighton & Hove Albion, in 1910, and this remains their only top level national honour.
In 1920, virtually the entire top division of the Southern League was absorbed by the Football League to become that league's new Third Division. A year later the Third Division was expanded and regionalised. The Third Division clubs from the previous season became the Third Division South, with the addition of the Third Division North.
For the next six decades, the Football League and Southern League would exchange a limited number of clubs as a result of the older league's re-election process. From 1920 onward, the Southern League's status as a semi-professional league was firmly established.
With its clubs seeking a more regular means of advancing to the Football League, in 1979 the Southern League became a feeder to the new Alliance Premier League along with the Isthmian League and the Northern Premier League, and the top Southern clubs of the day joined the new league. In turn, the APL (renamed Football Conference in 1986) would eventually succeed in becoming a feeder to the Football League. The league lost more of its top clubs in 2004 when the Conference added two regional divisions below the existing National League, the Conference South and Conference North.