The church dates from the early 12th century. The church became collegiate when Richard Whitton was appointed by the
Bishop of Durham Rt Revd Robert Neville as the first Dean of Darlington in 1439. To support the dean, there were four prebendaries, Cockerton, Newton, Blakwell and Darlington. The college survived until 1550 when it was dissolved. Following a lightning strike on the spire on 17 July 1750, the crossing tower was rebuilt in 1752. A major restoration took place in 1864-65 by the architects
George Gilbert Scott of London and
James Pigott Pritchett of Darlington. The estimated costs of the works were £1,590 () and
William Vane, 3rd Duke of Cleveland gave £500 () towards the restoration. The work involved removal of the galleries and ceilings, the opening out of the gable windows in the nave and transepts, the rearranging of the pews, and the replacing of several stalls which had been destroyed. The main work was the restoration of the chancel where the piscina and armoury were restored, the sedilia restored to their original depth, the floor laid with encaustic tiles and eleven stained glass windows inserted. A font was presented by R.H. Allan, of grey polished marble. A lectern by Messrs King and Collie of Durham was presented by Miss Topham. The organ was restored and the bells in the tower were recast. The church was reopened for worship on 14 December 1865. In March 2026, the remains of an earlier place of worship, thought to be
Anglo-Saxon and dating from circa
1080, was discovered beneath the floor of St Cuthbert's during restoration work; the remains are to be catalogued and preserved. ==Incumbents==