Ian Foster’s side have been the league’s in-form team, remaining unbeaten at home in all competitions and on a run of eight games without defeat.
They had to rely on the brilliance of goalkeeper Peter Cherrie to keep them in the game early on though, as he denied Gareth McGlynn from the spot after the Candystripes player had been pulled to ground inside the box by Michael Hector.
Stephen Kenny’s side should have taken the lead on 34 minutes when Ruairdhri Higgins’ volley from the edge of the area thundered back off the underside of the crossbar, and Eamon Zayed following up was somehow denied by a world-class stop from Cherrie.
Having survived that scare, Dundalk hit the front themselves two minutes before the break when Hawkins raced onto an inviting cross from Dean Bennett to send a bullet-like header to the top left-hand corner.
The Lilywhites were unlucky not to add to their advantage six minutes after the restart when Mark Quigley hit the inside of the post, while Zayed went close for Derry in stoppage time.
DUNDALK: Cherrie; Madden, Hawkins, Hector, N Murphy; Kearns, Bennett, Bolger, Ward, Quigley; Griffin (Breen, 89 mins).
DERRY CITY: Doherty, McCallion (McDaid, 67 mins), Greacen, S McEleney, Lafferty (Harkin, 82 mins); McClean, Higgins, Molloy, McLaughlin (P McEleney, 67 mins); McGlynn; Zayed.
Referee: D Hancock (Dublin).