The A4289 consists of two short Class I sections – either side of the town centre – of Swindon's Ring Road, almost all the rest of which is the B4289.
The route begins at the Kingshill Roundabout, at the south west-corner of the Ring Road, where it also meets the A3102. It runs east along Kingshill Road and Bath Road to reach Swindon's Old Town, where it turns south into Devizes Road, a fairly narrow shopping street. Within 300 metres this section ends, with the Ring Road turning left as the B4289 (Newport Street) and the southbound road ahead being the A4361 (Croft Road).
The second section of the A4289 starts at the Magic Roundabout, where the Ring Road meets the A4312. It heads north along County Road to the southern of a pair of roundabouts, one on each side of the railway overpass known as the Transfer Bridges. Here the A4313 comes in from the right and the A4311 continues north, passing under the bridge, with the Ring Road (once again the B4289) turning left from it at the northern roundabout.
The majority of the southern section of the A4289 was originally numbered A4015, with the exception of Devizes Road which was the A361. Upgrades to the Swindon's road network when it became a New Town downgraded this road to B-class status (possibly as part of the B4006), then it gained the A4289 number later on.
The northern section of the road was part of the original route of the A419, which became the A345 when the A419 moved onto the bypass and then the A4259 when that road was truncated south of the M4. In the 2000s the A4259 was cut back, allowing the A4289 to gain its separate section (the two roads don't join, however, as the A4312 has also taken over part of the ex-A4259).