Dave Webster fired home from 20 yards after fellow substitute Ismahil Akinade had laid on a perfect ball back into his path.
The Seagulls might have broken the deadlock on 13 minutes when a low cross from Marty Waters on the left allowed striker Jason Byrne to get in a shot deflected off Sean Whelan into the path of John Mulroy, only for the latter to shoot narrowly wide.
Both teams did have the ball in the net when first Derek Foran headed home for Dundalk and then Byrne was on target for Bray. Both efforts were correctly ruled out for offside.
Dundalk went close to grabbing the lead on 33 minutes when a corner by Mark Griffin on the left was powerfully headed goalwards by the unmarked Michael Rafter, only to be cleared for a corner by Mulroy with keeper Darren Quigley beaten.
Bray had chances early in the second half when first Waters fired over the top and then Adam Hanlon shot straight at Peter Cherrie from 12 yards.
The home side were to rue those misses as Dundalk opened the scoring on 55 minutes when substitute Lorcan Shannon swapped passes with Griffin to set up the chance for Gary Shanahan to fire home from close range.
The Seagulls did have chances late on when first Waters hit the post before a Mulroy effort was pushed round the post by the excellent Cherrie.
BRAY WANDERERS: Quigley; S O’Connor, Mitchell, D O’Connor, Massey; Hanlon (Marshall 64), Houston (Webster 75), K O’Connor, Waters; Byrne, Mulroy (Akinade 82).
DUNDALK: Cherrie, Mountney (McDonnell 70), Foran, Whelan, Osborne; Walsh (Shannon 53), Shields , O’Brien, Shanahan; Rafter (Woods 82), Griffin.
Referee: Derek Tomney (Dublin).