A baptism of fire awaits City’s new boss Tiernan Lynch, as the Candystripes will travel to Tolka Park to face Shelbourne on the opening night of the 2025 season.
The 2025 season kicks off on Valentines Night, but there will be no love lost between League of Ireland sides in the chase for honours.
Shels were crowned champions in the Brandywell in the final game of the 2024 season but City will have a chance to set down a marker with a trip to Dublin on the opening night.
The first home game in the Ryan McBride Brandywell Stadium will see City host Bohemians on the 21st of February.
| Round | Day | Date | Time | Opponent | Home/Away |
| 1 | Friday | 14/02/2025 | 19:45 | Shelbourne FC | A |
| 2 | Friday | 21/02/2025 | 19:45 | Bohemian FC | H |
| 3 | Friday | 28/02/2025 | 19:45 | Waterford FC | H |
| 4 | Monday | 03/03/2025 | 19:45 | St. Patrick’s Athletic FC | A |
| 5 | Friday | 07/03/2025 | 19:45 | Galway United FC | H |
| 6 | Saturday | 15/03/2025 | 19:45 | Sligo Rovers FC | A |
| 7 | Friday | 28/03/2025 | 20:00 | Shamrock Rovers FC | A |
| 8 | Friday | 04/04/2025 | 19:45 | Cork City FC | H |
| 9 | Friday | 11/04/2025 | 19:45 | Drogheda United FC | H |
| 10 | Friday | 18/04/2025 | 19:45 | Galway United FC | A |
| 11 | Monday | 21/04/2025 | 17:00 | Sligo Rovers FC | H |
| 12 | Friday | 25/04/2025 | 19:45 | Waterford FC | A |
| 13 | Friday | 02/05/2025 | 19:45 | Shelbourne FC | H |
| 14 | Monday | 05/05/2025 | 17:00 | St. Patrick’s Athletic FC | H |
| 15 | Friday | 09/05/2025 | 19:45 | Cork City FC | A |
| 16 | Friday | 16/05/2025 | 19:45 | Drogheda United FC | A |
| 17 | Friday | 23/05/2025 | 19:45 | Shamrock Rovers FC | H |
| 18 | Friday | 30/05/2025 | 19:45 | Bohemian FC | A |
| 19 | Friday | 13/06/2025 | 19:45 | Galway United FC | H |
| 20 | Friday | 20/06/2025 | 19:45 | Shelbourne FC | A |
| 21 | Monday | 23/06/2025 | 19:45 | St. Patrick’s Athletic FC | A |
| 22 | Friday | 27/06/2025 | 19:45 | Drogheda United FC | H |
| 23 | Friday | 04/07/2025 | 19:45 | Waterford FC | H |
| 24 | Saturday | 12/07/2025 | 19:45 | Sligo Rovers FC | A |
| 25 | Friday | 25/07/2025 | 19:45 | Bohemian FC | H |
| 26 | Friday | 01/08/2025 | 20:00 | Shamrock Rovers FC | A |
| 27 | Friday | 08/08/2025 | 19:45 | Cork City FC | H |
| 28 | Friday | 22/08/2025 | 19:45 | Galway United FC | A |
| 29 | Friday | 29/08/2025 | 19:45 | St. Patrick’s Athletic FC | H |
| 30 | Friday | 12/09/2025 | 19:45 | Bohemian FC | A |
| 31 | Friday | 19/09/2025 | 19:45 | Shelbourne FC | H |
| 32 | Friday | 26/09/2025 | 19:45 | Drogheda United FC | A |
| 33 | Friday | 03/10/2025 | 19:45 | Sligo Rovers FC | H |
| 34 | Friday | 17/10/2025 | 19:45 | Waterford FC | A |
| 35 | Friday | 24/10/2025 | 19:45 | Shamrock Rovers FC | H |
| 36 | Saturday | 01/11/2025 | 19:45 | Cork City FC | A |
