A handful of Avanti West Coast services also serve the station, but these have been greatly reduced due to the longer-term impact of the COVID-19 pandemic in the United Kingdom.

Although the promoters of the London and Birmingham Railway had considered routes passing close to Northampton in 1830, the town was skirted by the final choice of alignment via Blisworth and a loop line to remedy this had to wait for several decades.

[5][6] The 120 ft (37 m) difference in gradient in the 4 mi (6.4 km) between Northampton and Blisworth, on the floor of the Nene Valley, is likely to have played a key role in the decision.

[7] The town was considered as the southern terminus of the Midland Counties Railway in 1833 but lost out to Rugby on account of the shorter distance with Leicester.

[9] Following the discovery of a large quantity of ironstone in Northamptonshire in 1851, a proposal was made by the London and North Western Railway (L&NWR) for an 18 mi (29 km) line from Market Harborough to Northampton which received Parliamentary approval in 1853.

[14] It would be the most basic structure on the line with no goods facilities, limited passenger waiting accommodation and an awning over the single platform.

[17][18][19][20][21] It was described in the L&NWR's minutes as a "very unassuming edifice", giving the impression that it was "merely temporary in nature" until traffic developed to a sufficient level to allow a "more imposing" structure to be built.

[22] The advent of the Great Northern and London and North Western Joint Railway to tap the coalfields of Nottinghamshire and Yorkshire led the L&NWR to quadruple its main line between Bletchley and Rugby and also to consider ways in which Northampton might be better served.

[24] The result of these works would be to put Northampton on an important coal artery from Nottingham and the North to the L&NWR's Camden goods depot.

[30] The main station building, a two-storey structure in the Italianate style, was located on the up side and consisted of a central block with two cross-wings.

[40] The station was chosen by British Rail for complete rebuilding in 1965–66 to designs by the architect Ray Moorcroft, as part of the electrification of the West Coast Main Line between Euston and Liverpool.

[43] The current was switched on for the first time between Hillmorton Junction to Northampton on 6 June 1965 for insulation tests, with steam locomotives being withdrawn from the area on 27 September 1965.

[42] Following the designation of Northampton Waterside as an enterprise zone in August 2011,[44] plans to replace the existing station with a new two-storey glass and steel structure were approved by the West Northamptonshire Development Corporation.

[49] Construction work was preceded by a three-month archaeological excavation by a team of specialists from the Northampton office of MOLA on the footprint of the new station building.

[58] The plans did not proceed due to the impact of COVID-19, the Russian invasion of Ukraine and cost inflation,[59] resulting in the Council reaching agreement in June 2023 with Network Rail and its development partner on the delivery of the car park.

As part of the re-development in 2015, there were proposals to build a multi-storey car park with direct access to the station; in June 2020 it was suggested that this will be put in place "in the not-too-distant future.

[63] The majority of services along the Trent Valley Line to Crewe, via Nuneaton and Stafford, run on the faster, more direct route between Milton Keynes Central and Rugby; this arises from London Midland's decision to run 110 mph regional services on the main spine of the West Coast Main Line.

[65] Avanti West Coast operates one train per early weekday morning to London Euston that stops here; this service originates from Edinburgh Waverley.

[68] The stock level rose under British Railways when it comprised 8Fs, 4Fs and LNWR 0-8-0s for freight workings, 'Black Fives', 2-6-2Ts and 4-4-0s for passenger services, while a few 3Fs and a single Webb 2-4-2T were used for shunting.

[68] A rearrangement of the offices and stores took place in 1927 under the London, Midland and Scottish Railway at a cost of nearly £1,000; the roof was also replaced by one with a 'louvre' pattern.

[70] Built at a cost £31m, it was constructed on a long, narrow strip of land previously the site of overgrown railway sidings.