Tommaso Orsini, Count of Manoppello sold this relic of the presumed veil of the Virgin to the friars of San Francesco in 1414.  It was subsequently displayed for veneration on the Feast of the Annunciation.   The original location of this display seems to have been the Cantoria dei Nepis (a chapel in the narthex of the lower church of San Francesco. 

The open loggia on the left of the facade of the upper church was first documented in 1589 as the place from which the Sacro Velo  was displayed for veneration on the second day of Pentecost.  (Its attribution to the Perugian Valentino Martelli in 1607, while ubiquitous, is incorrect).

From ca. 1595, the display was followed by a procession to Santa Maria degli Angeli, where the relic was displayed from a loggia on the facade of the new church.  This fresco (late 16th century) in the Cappella del Presepio there,  which is [attributed to] Silla Piccinini, depicts this procession.  

Camilla Peretti, the sister of Pope Sixtus V gave to the friars a new  silver reliquary (1604) for the relic, which was subsequently housed in the new Altare delle Reliquie (1607).  This altar was demolished in ca. 1870, when the relic was moved to the Sacristy.

The bronze relief that covers the funerary niche above the altar of the Cappella di San Giovanni Battista was installed in 1926, when the Sacro Velo della Madonna was placed here.