Plymouth City Council has a large and important fine art collection. With over 900 paintings, 3,000 watercolours and drawings, over 5,000 prints and small collections of sculpture and miniatures, it represents the largest fine art collection in Devon and Cornwall. The works span the 16th to 21st centuries and include examples from a wide range of European schools. The vast majority are English and date from the 19th and 20th centuries.

Within the art collections, but retained as a separate entity is the Cottonian collections. This designated collection contains small groups of ceramics, bronzes and paintings, several hundred Old Master and English drawings and watercolours, and a substantial body of several thousand fine and rare prints. Together with a sizeable library of some 2,000 tomes, this outstanding collection is of international importance. Initiated in the late 1740s by Charles Rogers, who amassed a substantial quantity of prints and drawings, it was passed through three successive generations of the Cotton family until it was finally opened as a public collection in 1853. This was transferred to Plymouth Corporation in 1915/1916 by an Act of Parliament.

The museum also manages collections on behalf of the city and lends substantial works to other venues including at: Port Eliot, St Germans, Cornwall (23 portraits acquired through the Acceptance in Lieu Scheme and on long-term loan to the estate. 14 are painted by Sir Joshua Reynolds); Civic Collections, Plympton St Maurice Guildhall and Plymouth City Guildhall, the Council House, and 3 Elliot Terrace (former home of Lady Astor and now the official residence of the Lord Mayor of Plymouth); Mount Edgcumbe House, Cornwall, portraits and landscapes relating to the site and the Edgcumbe family.