The library's construction and maintenance was funded from the estate of John Radcliffe, a notable doctor, who left £40,000 upon his death in 1714. According to the terms of his will, construction only began in 1737, although the intervening period saw the complex purchase of the site. The exterior was complete in 1747 and the interior finished by 1748, although the library's opening was delayed until 13 April 1749.

Upon completion, Francis Wise was appointed as its first librarian. Until 1810, the library housed books covering a wide range of subjects, but under George Williams it narrowed its focus to the sciences. Williams brought the library from a state of neglect up to date, although by 1850 the Radcliffe Library still lagged behind the Bodleian. It was at this point that Henry Wentworth Acland, then librarian, laid out plans for the Radcliffe Library building to merge with the university and the library's collection of books to be moved to the newly constructed Radcliffe Science Library, which were accepted by the library's trustees and the university. It was at this point that the building became known as the Radcliffe Camera, serving as a reading room for the Bodleian. Some visitors and tourists erroneously believe the Radcliffe Camera houses the Bodleian's collection of rare books; however, a large collection of rare and antiquarian books are contained in the nearby Weston Library and there are in excess of 1 million searchable records online for books, journals, magazines, newspapers, maps, ephemera, and music printed before 1900 covering antiquarian collections held in almost 60 libraries in Oxford.

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