The first Borough Charter was granted to Denbigh in 1290, when the town was still contained within the old town walls. During the Wars of the Roses, the town was largely destroyed, subsequently moving from the hilltop to the area of the present town market. In 1643, Denbigh became a refuge for a Royalist garrison during the English Civil War. Surrendering in 1646, the castle and town walls eventually fell into ruin.
Notable buildings in Denbigh include Denbigh Castle, the town walls begun in 1282 including the Burgess Gate, and Leicester's Church. This is an unfinished church begun in 1579, planned as a cathedral with the title of city to be transferred from neighbouring St. Asaph. The project ran out of money and the grounds now lie derelict. Other attractions in the town include a library & museum.
Denbigh was once served by a railway station on the former London and North Western Railway, later part of the LMS. The "Vale of Clwyd" line leading north to St. Asaph and Rhyl closed in 1955, leaving Denbigh on a lengthy branch running from Chester via Mold and Denbigh to Ruthin, which closed in 1962. A southern continuation beyond Ruthin linking up with the Great Western Railway at Corwen had closed in 1952. The platform of Denbigh station can still be seen beside the road leading to the Kwik Save store.
Denbigh hosted the National Eisteddfod in 1882, 1939 and 2001.
At one time the majority of the population sought employment at the North Wales Hospital, which cared for people with psychiatric illnesses. The hospital closed in the late 1990s.
Denbigh Cricket Club is one of the oldest cricket clubs in Wales having been established in 1844. The club plays at the Ystrad Road ground and plays in the North Wales Cricket League. The 1st X1 play in Division 1 with the 2nd X1 in Division 3.