National League North and South clubs enter the competition in the second qualifying round stage, with National League sides joining in at the fourth round of qualifying.
The extra-preliminary, Merseyside derby tie between Litherland REMYCA and AFC Liverpool this Saturday (12.30pm kick-off) is the first game set to be shown.
The matches can be watched live on PC, mobile or connected TVs and will be available live and on-demand on BBC iPlayer.
Steve Rudge, BBC Sport's head of football, said: "We are delighted that audiences will be able to share in the passion of the FA Cup from the opening stage of the competition for the very first time. To highlight the tournament from first kick to last will showcase the desire for success in the famous Cup throughout the football pyramid."
David Newton, the FA's head of competitions, said: "The Emirates FA Cup is the world's most loved domestic cup competition, and it kicks off this weekend with 185 fixtures.
"We're delighted that the BBC is widening the competition's reach by allowing fans the opportunity to follow the drama live, right from the very start on Saturday through to the showpiece final at Wembley Stadium next May."
Key FA Cup dates for National League teams:
Second Round Qualifying - Saturday 16 September 2017
Third Round Qualifying - Saturday 30 September 2017
Fourth Round Qualifying - Saturday 14 October 2017
First Round Saturday - 4 November 2017