The Aylesbury and Buckingham Railway Company was incorporated on 6 August 1860,
 and the line opened on 23 September 1868 connecting
Verney Junction and serving intermediate stations at
Waddesdon Manor (renamed Waddesdon on 1 October 1920),
Quainton Road, Grandborough (renamed
Granborough Road on 6 October 1920), and
Winslow Road. The A&BR was never extended to Buckingham.
In the late 1880s the
Metropolitan Railway planned to extend its projected Aylesbury line northwards to
Morton Pinkney, to make a junction with the
East and West Junction Railway. Instead, the Aylesbury and Buckingham Railway Company was absorbed by the Metropolitan Railway on 1 July 1891 and it thus formed the northward progress of the Metropolitan Railway.
The section of line from Morton Pinkney to just north of Quainton Road railway station was built later as part of the London Extension of the
Great Central Railway, joining the, by then, Metropolitan Railway tracks into London, and forming the
Great Central Main Line which opened for passenger traffic on 15 March 1899.
In April 1906 the Metropolitan Railway section from
Harrow-on-the-Hill station to Verney Junction was leased to a Joint Committee of the Metropolitan Railway and Great Central Main Line: it was worked on a five-yearly basis alternately by the joint lessees.
Passenger services on the line were withdrawn between Quainton Road and Verney Junction from 6 July 1936, and the intermediate stations of Granborough Road and Winslow Road closed. The last through service, a parcels train from Verney Junction, was on 6 September 1947.