From north to south, the road begins at Wicksteed Park in the outskirts of Kettering. It then crosses the A14 (where it becomes a primary route) and goes through Isham and Great Harrowden. After this it goes on to form the Wellingborough western bypass before leaving Northamptonshire to cross into the Borough of Milton Keynes (ceremonial Buckinghamshire). From there, it crosses the A428 at a roundabout and cuts through the centre of Olney. South of Olney the road passes Emberton, meeting the A422 just east of Newport Pagnell, where the routes multiplex to form the Newport Pagnell eastern bypass. South of Newport Pagnell, the routes diverge at a roundabout with the A509 turning south and the A422 continuing westbound. Here the A509 is a single carriageway once more until it crosses the M1 at Junction 14, where it enters Milton Keynes proper and multiplexes for a short distance with the A4146 (on separating, the latter takes over the 'primary route' designation and the A509 loses it). Once more a dual carriageway, it runs for a further 4 miles (6.4 km) past the edge of Central Milton Keynes (the central business district) and the Network Rail National Centre ('Quadrant:MK'), to link up finally with the A5. Through Milton Keynes the road is known as the H5 Portway.
During 2005 there were two fatal crashes in the same 100m stretch of the road as it passes between Emberton and Petsoe End. This area of the road had become notorious as a black spot for traffic accidents, and residents of Emberton had complained to Milton Keynes Borough Council for a number of years for improvements to the road. In July 2005 local residents met in the village and demanded a 40 mph (64 km/h) speed limit and improvements. These were promised by the Council within six months, but were implemented in September 2006.