The ruins of the church centre around a rectangular structure with N and S additions. Dates in the 16thc and 17thc for the primary post-Reformation additions have been suggested, but there is no surviving documentation concerning this work. Major construction on the the church is only first recorded for 1739-40, when certain renovations were carried out. Minor repair and maintenance is documented in succeeding decades, including for replastering in 1776, but no major construction is recorded after 1740. Following much consideration in the early 19thc about the cost of renovating the church, it was decided to rebuild on a completely different site. The new church was begun in 1818.

During the 1993 excavations, earlier activity beneath the church was found, but there was no evidence of a pre-Romanesque church. Foundations of the Romanesque church were discovered with a chamfered plinth beneath the N and S walls and for the original W wall, which was further E than at present. These showed that the first church was about half the length of the present structure.

Within the surviving nave walls of the church are reused stones from the Romanesque church. Other carved stonework, with roll mouldings, survive and are laid out in the E part of the church, now overgrown. There is also a single head of beakhead form built into the E exterior of the S extension.

There is no mention of Cockpen Church in the 12thc, but in 1356 Patrick de Ramsay granted the church at Cockpen to Newbattle Abbey. The Ramsays were lords of Dalhousie, with their main castle nearby. The first record of a Ramsey family member is that of Simon de Ramsay (Simundus de Ramesie), who appears in a documents in Scotland c.1140. It has been suggested that he followed David I from Huntingdonshire to Scotland sometime between 1124 (when David became king) and 1140. Although no documents concerning the construction of the medieval church survive, it is thought that the E end was extended in the 13thc and the W end in the 14thc.

The history of the Ramsays makes it not unlikely that they were responsible for the construction of the church, with a probable date in the 2nd quarter of the 12thc. The lack of documentation for the church, however, means that a date in the 3rd quarter of the 12thc cannot be ruled out.

One of the most intriguing stones is that carved with a kind of beakhead. Beakhead is not common in Scotland, though it was used occasionally in the SW part of present-day Scotland and in Cumbria, a large section of which was under the control of the Scottish king for part of the 12thc. It was also used later in the century on the W doorway of Kelso Abbey Church.

The voussoirs with roll mouldings, now on the ground at the E end of the ruins, come from a substantial arch, one possibility for which is the chancel arch. Most Romanesque roll mouldings have a concave section next to them, but roll mouldings flanked by chamfers similar to those found at Cockpen did occur by at least the mid-12thc in Scottish architecture (as in the E end of Jedburgh Abbey). Nonetheless, most examples of the Cockpen type tend to be of late-12thc date or even later. A comparison with the moulding carved around the interior of the E ocular window at Cockpen (probably 13thc) may suggest that these are of a similar period. There must, however, remain at present a question about their date.

The roll-moulded voussoir with significant paint still on it, built into the S wall of the S extension, is not the same as the other roll-moulded voussoirs, as it has a large lower chamfer and seems to have a slightly larger roll. It must have come from a different arch and may have been used somewhere on the interior of the church (judging by the surviving paint), but its date and original location remain uncertain.