The new "phoenix" club have been placed by the FA in Division One of United Counties League.
AFC R&D will play at Wellingborough Town's Dog and Duck ground for their first season in senior football.
Rushden Town last played in the UCL in 1982-83 when they were promoted to the Southern League. Irthlingborough Diamonds last played in the UCL in 1991-92 after which the two clubs merged.
Rushden & Diamonds rose to the dizzy heights of the old Football League Second Division where they rubbed shoulders with the likes of QPR, Blackpool and Sheffield Wednesday in 2003-04 - before being relegated back to the Conference and going bust last year.
The FA have also confirmed the promotion of runners-up King's Lynn Town, who are likely to play in the Ryman League Division One North.