London-born, Mr Humphreys (59) is now a lecturer at the Otago Polytechnic School of Art.
He staged his first exhibition in the foyer of the Otago Museum in 1978.
During that show, "Sonia", an escaped circus lioness who is now one of the attic's favourite inhabitants, was brought to the museum for the first time.
Thus began his fascination with the attic, which is believed to be the only surviving Victorian-style museum gallery in the country.
"It's my favourite museum space in New Zealand," he adds.
Created in 1878, the attic later fell into disuse for more than a decade before being restored and reopened to the public in 1996.
Mr Humphreys has created two large diptych paintings, both acrylic on canvas, which are displayed in the attic's raised central area.
Other "drawings, silhouettes and objects', including a dense flock of black parrots, have slipped into many of the glass cases, which already displayed a host of museum-dwelling animals - many of them stuffed - which once crept, ran, flew or swam.
The exhibition, which runs until April 26, had much earlier origins, with Mr Humphreys beginning its initial paintings in 2003 as a personal response to the Animal Attic.
The paintings explored "the shallow and sometimes claustrophobic space of the glass case", he said.
The qualities of "formal stillness and silence" present in the "ordered archive of the museum" also suggested links with "the rituals that pervade our everyday existence, particularly the rituals based around experiences of loss".
Titled "Art in the Attic: Sheet Music (for Cheryl)", the exhibition is dedicated to his late wife, Cheryl Humphreys.
Through the exhibition, he was reconnecting the museum with the living world of the commonplace, and with "implications of mutuality and interdependence" that could be considered alternately as "humorous or tragic", he said.
