Beginning in Honiton at the eastern junction with the A30 road,[2] the A35 travels in a roughly south-easterly direction past Axminster, Charmouth and Bridport.

After Dorchester, there are approximately 8 miles (13 km) of dual carriageway, including the Puddletown bypass, until it reaches its roundabout with the A31 road at Bere Regis.

[6] This added the narrow 220-foot (67 m) long Charmouth Tunnel to the route, built in 1832 to avoid the summit of Thistle Hill.

A much-desired southern bypass for the town was indefinitely postponed in 1980 by the then Parliamentary Under-Secretary of State for Transport, Kenneth Clarke.

[17] In October 2021 the edge of the eastbound carriageway collapsed into a field where the A35 ascends an escarpment 1.1 miles (1.8 km) east of Honiton.

Due to the complex ground conditions repairs took 8 months to complete with temporary signals controlling single-file traffic for that time.