The last attempt to create a fully national league underneath the had been the , which was absorbed as in 1892.
The league was formed as the Alliance Premier League in 1979, coming into force for the . The league drew its clubs from the Northern Premier League and the .
It greatly improved the quality of football at this lower level, as well as improving the financial status of the top clubs. This was reflected in , when the Football League began accepting direct promotion and relegation between the Conference and the bottom division of the Football League, which at that time was known as the and is now EFL League Two. The first team to be promoted by this method was Scarborough, whereas the first team relegated was Lincoln City, who regained their Football League status a year later as Conference champions.
Since , the league has been granted a second promotion place, with a play-off deciding who joins the champions in the EFL. Previously, no promotion from the Conference would occur if the winners did not have adequate stadium facilities. As of the start of the 2002–03 season, if a club achieves the automatic promotion or the play-off places but does not have an adequate stadium, their place will be re-allocated to the next highest placed club that has the required facilities.
In , the Conference increased its size by adding two lower divisions, the Conference North and Conference South respectively, with the original division being renamed Conference National. For the , the Conference National expanded from 22 to 24 teams by promoting four teams while relegating two teams and introduced a "four up and four down" system between itself and the Conference North and Conference South.