National League chief executive Michael Tattersall will leave the role, and the organisation, at the end of December.
The 45-year-old was appointed in November 2015 after 12 years with the English Football League.
The National League said Tattersall had overseen "a period of sustained growth of the competition, increasing its profile and commercial value".
He was also involved in the introduction of a six-team play-off system for promotion to the EFL.
National League chairman Brian Barwick said Tattersall had served the league and its member clubs with "great distinction".
"He has shown outstanding professionalism and a comprehensive understanding of the sport, its competitive framework and associated business," Barwick added.
Analysis - Funding allocation questioned
BBC Sport's Simon Stone
Whilst the National League has enjoyed growth under Tattersall, in recent weeks there has been growing discontent over the method in which government funding was distributed to the clubs.
The government gave £10m to the league in October to allow its season to start behind closed doors.
However, rather than make payments based on the likely losses had attendances matched those of previous seasons, only four sizes of payment were made, ranging from £95,000-per-month to £30,000-per-month.
Whilst the best supported clubs in each of the National League's three divisions - National League, National League North and National League South - have been placed in the higher bracket, they felt the move disadvantaged them.
Notts County's £95,000-per-month payment equates to £18.23 per fan on their 5,210 average home gate last season.
For Boreham Wood, their £84,000-per-month is £116.02 for each of the 724 average fans they had for home league games.
In addition, there was confusion over the failure of Havant & Waterlooville to gain permission for fans to enter their stadium for Wednesday's National League South fixture with Hemel Hempstead Town.
The club said they had been working all week to make their ground Covid secure but "despite the club undertaking everything possible to get fans in", approval had not been granted by the National League.