While construction was proceeding under Wylie & Peddie, the KR concluded an agreement with the G&SWR for the latter to work the line for 42½% of gross receipts after deduction of cartage costs.

The line opened to goods traffic on 17 February 1864 but the Board of Trade (BoT) Inspecting Officer declined to authorise passenger operation until the junction with the Portpatrick Railway was improved.

The line opened to passengers on 2 March 1864 between Kirkcudbright and a quickly-constructed station at St Andrew Street, Castle Douglas, short of the junction.

The planned entry to the junction at Castle Douglas was extremely sharp; and Kirkcudbright trains entering the station had to use a short length of Portpatrick Railway track; it appears that permission for this had not been properly obtained.

Signalling alterations were made at the Castle Douglas junction and a low speed restriction imposed, and through passenger running commenced on 15 August 1864.

The line ran north from Kirkcudbright, crossing the river at Tongueland Bridge (later spelt Tongland) and keeping to the west of the ridge that forms Bar Hill.

Improvements to the layout at the station took place some time before 1894, and the Kirkcudbright line then entered independently by a more gentle alignment, passing under a separate span of Dumfries Road bridge, which was widened for the purpose.