Aylesbury Town Council serves the residents of the parish of Aylesbury Town and is the first tier of local government. Independent from the two other Councils in Aylesbury, Aylesbury Vale District Council and Bucks County Council, the Town Council provides a number of different services to the people of Aylesbury. These include maintenance and administration of the public cemetery on Tring Road, maintenance and administration of the seven allotment sites around the town, grants to organisations benefiting the people of Aylesbury or promising young sports people, a diverse range of free events such as Aylesbury on Sea, Soapbox Derby, Parklife and many more. The Council contributes to planning and licensing by commenting on applications to the planning authority.
The Town Council also looks after the Mayor's office, who is elected once a year in May.

Aylesbury Town Council has also taken on devolved services from Buckinghamshire County Council for the cutting of grass verges.

The Council also operates and manages the Jonathan Page Play Centre and offers an After School Club and Holiday Playscheme for children from the age of 4 up to their 13th birthday.

The Town Council consists of 25 Councillors covering 13 wards (Quarrendon, Gatehouse, Elmhurst, Oakfield, Bedgrove, Mandeville and Elm Farm, Walton Court, Southcourt, Oxford Road, Coppice Way, Walton, Hawkslade and Central). The Councillors are elected every 4 years. The next election will be in 2020.