Francis Thompson is believed to have been the architect of this distinctive station building, but Sancton Wood and Henry Hunt may also have played a part. It was opened in 1845 by Eastern Counties Railway with a single platform as was common practice at that time. In 1848 a second platform appeared, made of wood, but it lasted only a year. It reappeared in 1850, but access over a bridge with extremely steep steps was so unpopular that the platform was removed in 1863.

Subsequently the long single platform has continued, though it has been supplemented by bay platforms at either end. These were originally used by Great Northern and London & North Western trains at the southern end and Midland and Great Eastern branch line trains at the northern end.

At 514 yards, Cambridge has the third longest railway platform in the country (after Colchester and Gloucester). The scissors crossover in the middle divides it in two, permitting trains from both directions to pass trains already stopped there. The section south of the crossover is platform 1 (alongside bay platforms 2 and 3), and the section north is platform 4 (alongside bays 5 and 6).

The station's distance from the centre of the city, about 1.5 km, owe as much from opposition by university authorities in the 19th century as to engineering factors. The G.E.R. maintained a special locomotive for the Royal Train here. Signal boxes in the station area were converted to electric operation in the 1920s by LNER. During the 1980s British Rail made some major refurbishments, including putting plane glass in the 15 arches of the colonnade, which restored the station to something approximating its appearance when first built.

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