The long history of the Biblioteca Capitolare of Verona begins around the year 380 as a storage area for religious manuscripts and then a library workshop operated by local priests.

The oldest dated document, known as Urcisinus Codex, reports the date of August 1, 517. The presence of a date is itself a rare feature for the time, but it allows to give the scriptorium a minimum certain age of at least 1500 years, making it the oldest library still in operation in the world. During the following centuries and throughout all the Carolingian epoch the scriptorium was very active in its document transcription and calligraphic work.

Dating back to this period, more precisely around the 8th or early 9th century is the so-called Veronese Riddle (Indovinello Veronese). This riddle, popular at the time and in the following centuries, was written in late Vulgar Latin on the margin of a parchment of a prayer book, and it is considered to be the earliest existing document in the Italian language.

The scriptorium became a proper library in the modern sense of the word starting from the 13th century, as the calligraphic work was becoming less important. It is also reported that during the 14th century, two of the most famous Italian writers of that period and of all time, Dante Alighieri and Petrarch, visited the library. Some of the earliest printed books in Italy, dating back to the mid 15th century are also stored here.

Even after being damaged by a flood in 1882, in which thousands of manuscripts were covered in mud, and being bombed in 1945 during World War II, the library is still standing and operating to this day, more than a millennium and a half since the beginning of its history.