Ciaran Kilduff struck an injury time equaliser as Shamrock Rovers grabbed a share of the SSE Airtricity League spoils at Tallaght Stadium.
The opening period was all about Derry City’s organisation as Roddy Collins’ charges stifled Rovers.
Within three minutes of the restart a freak goal from Mark Stewart edged the Candystripes ahead.
Ryan Brennan, Gary McCabe, and substitute Stephen McPhail all went close for Rovers, who eventually scored four minutes into stoppage time courtesy of a Kilduff header.
Though Shamrock Rovers had a few early set-piece opportunities Derry came close to nicking a goal from a ninth minute breakaway.
Promising youngster Enda Curran dragged a right-footed effort wide from the edge of the area as the Candystripes sought to land a blow.
Surprisingly, the remainder of the first half was short on goalmouth incident as Derry’s midfield diligence frustrated Rovers.
Shane McEleney was effective in a new role anchoring the Derry midfield, while Danny Ventre and Barry Molloy were also industrious for the visitors.
Safe and solid Derry, with skipper Cliff Byrne supplying the defensive experience, got to the interval still on terms.
In the 48th minute the complexion of the game altered significantly as Derry took the lead in strange circumstances.
Stewart’s right wing cross deceived Rovers’ custodian Barry Murphy and suddenly Derry were protecting a lead.
For a spell Rovers improved as they tried to involve Kieran Marty Waters, but Derry continued to be resilient with Ventre impressive.
Ger Doherty made two splendid reflex saves to thwart Ryan Brennan and Gary McCabe as the Hoops pressed for an equaliser.
Trevor Croly introduced Stephen McPhail in an attempt to provide subtlety to the Rovers midfield, but Derry remained defiant.
Late on, McPhail dragged a shot wide but Rovers were fortunate to survive a scare themselves when Murphy saved from replacement Rory Patterson.
But Rovers kept battling and four minutes into additional time Kilduff climbed highest in the area to nod home Brennan's delivery.
Shamrock Rovers: Barry Murphy; Rob Cornwall, Conor Kenna, David O’Connor (Jason McGuinness, 64), Luke Byrne; Gary McCabe (Ronan Finn, 78), Robert Bayly (Stephen McPhail, 53), Ryan Brennan, Kieran Marty Waters; Eamon Zayed, Ciaran Kilduff. Subs not used: Craig Hyland, Karl Sheppard, Dean Kelly, Sean O’Connor.
Derry City: Ger Doherty; Roddy Collins Junior, Aaron Barry, Cliff Byrne, Ryan McBride; Shane McEleney (Patrick McEleney, 57); Mark Stewart, Danny Ventre, Barry Molloy, Michael Duffy (Ryan Curran, 89_; Enda Curran (Rory Patterson, 57). Subs not used: David Elebert, Dean Jarvis, Raymond Fox, Michael Lynch.
Referee: Paul McLaughlin.