Starting at the seaside resort of Margate at the north-east point of Kent, the A28 runs inland and west-southwest to the cathedral city of Canterbury, before passing through the chalk hills of the North Downs via the gap cut by the River Stour, to the town of Ashford in the Vale of Holmesdale.

The A28 leaves Margate via the seaside resorts of Westgate and Birchington, and then heads inland reaching open countryside at the village of Sarre, after which the road roughly parallels both the Ashford-Ramsgate railway line and the Great Stour river on their combined route to Canterbury and then Ashford.

It forms part of Canterbury's ring road before leaving via Wincheap and Thanington Without, where a sliproad linking to the A2 was completed in 2011.

In 1983, this section was named Simone Weil Avenue, in honour of the French philosopher and mystic who is buried nearby in Bybrook Cemetery.

The A28 continues via the villages of Rolvenden and Newenden before crossing a narrow bridge over the River Rother and entering East Sussex via Northiam, beyond which the road becomes very winding.