The Kendal & Windermere was promoted because of concerns that the Lancaster and Carlisle Railway (which now forms part of the West Coast Main Line from London to Glasgow) was not planned to go via Kendal. Although a 3.5 km tunnel north of Kendal was proposed to allow the L&CR to be routed via Kendal, that was too expensive, and the line seen today was adopted, running 1.5 km east of Kendal and then turning north-east.

As a result, efforts were put towards a branch line from the L&CR at Oxenholme, to run through Kendal to Windermere. In this context, "Windermere" meant the lake, the Windermere station terminus being at the village of Birthwaite about one kilometre from the lake, the village only later becoming known as Windermere. Oxenholme's railway station is now known as 'Oxenholme Lake District' because of the branch line.

There was opposition to the proposals from those who were against what they saw as destruction of the Lake District landscape. Those opposing included the poet William Wordsworth. His letters to the editor of the Morning Post are reproduced in The Illustrated Wordsworth's Guide to the Lakes, P. Bicknell, Ed. (Congdon and Weed, New York, 1984), pp. 186-198. His reactions to the technological and "picturesque" incursions of man on his beloved, wild landscape most famously include the following sonnet:

Is then no nook of English ground secure
From rash assault? Schemes of retirement sown
In youth, and 'mid the busy world kept pure
As when their earliest flowers of hope were blown,
Must perish;—how can they this blight endure?
And must he too the ruthless change bemoan
Who scorns a false utilitarian lure
'Mid his paternal fields at random thrown?
Baffle the threat, bright Scene, from Orresthead
Given to the pausing traveller's rapturous glance:
Plead for thy peace, thou beautiful romance
Of nature; and, if human hearts be dead,
Speak, passing winds; ye torrents, with your strong
And constant voice, protest against the wrong.
Despite this opposition, the Kendal and Windermere Railway Act authorising construction received the royal assent on 30 June 1845, and when the L&CR opened southwards from Oxenholme on 22 September 1846, the route to Kendal was already built. By 20 April 1847, the through route to Windermere station was complete.

The railway was leased in perpetuity to the Lancaster & Carlisle on 3 May 1858; the following year, the L&CR was leased to the London and North Western Railway, which put the whole of the West Coast Main Line under their control; in 1923 the LNWR became part of the London, Midland and Scottish Railway.

The branch had a variety of through services at various dates, including to London, Manchester, Preston, Grange over Sands, as well as many special excursion trains. In 1966 it was reduced to a local service only (to/from Oxenholme), and on 3 August 1968, the last steam train ran on the line. Goods traffic on the branch finished in 1972. The double-track branch became single-track in 1973 to save money. With the West Coast Main Line electrified, consideration was given to electrifying the branch, but this was not carried out.

In 1994, the branch began what may be seen as a renaissance, with through trains introduced to Manchester Airport, which continue today, though they are now run by TransPennine Express.

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