Updated list based on all of the input given in this thread. This thread is definitely not complete: I already know there are a few missing on here, and likely some outdated listings as well. Updates and background research is encouraged; I will also work on this.
I've also decided to include all non-AZA zoos in the US and Canada, so feel free to include information from zoos previously not considered. As for insectivorous bats, I'm only going to list them if the zoo has a confirmed breeding group; rehab individuals cycle in and out too often for us to keep an accurate track.
Rodrigues flying fox, Pteropus rodricensis
Akron Zoo
Bronx Zoo
Brookfield Zoo
Central Park Zoo
Cleveland Metroparks Zoo
Disney’s Animal Kingdom
Lincoln Children's Zoo
Louisville Zoo
Lubee Bat Conservancy
Moody Gardens
Oregon Zoo
Philadelphia Zoo
Prospect Park Zoo
Pueblo Zoo,
Riverbanks Zoo
San Diego Safari Park
Large/Malayan flying fox, Pteropus vampyrus
Busch Gardens Tampa
Columbus Zoo
Disney's Animal Kingdom
Lowry Park Zoo
Lubee Bat Conservancy
National Aviary in Pittsburgh
Oakland Zoo
Indian flying fox, Pteropus giganteus
Baton Rouge Zoo
Boise Zoo
Bronx Zoo
Cincinnati Zoo
Houston Zoo
Lubee Bat Conservancy
Metro Richmond Zoo
Omaha’s Henry Doorly Zoo
Point Defiance Zoo & Aquarium
Sedgwick County Zoo
Topeka Zoo
Woodland Park Zoo
Island flying fox, Pteropus hypomelanus
Brevard Zoo
El Paso Zoo
Lubee Bat Conservancy
Oakland Zoo
Turtle Back Zoo
Little golden-mantled flying fox, Pteropus pumilus
Columbus Zoo
Lubee Bat Conservancy
Omaha's Henry Doorly Zoo
Grey-headed flying fox, Pteropus poliocephalus
Lubee Bat Conservancy
National Aquarium in Baltimore
Spectacled Flying Fox Pteropus conspicillatus
Lubee Bat Conservancy
Straw-colored fruit bat, Eidolon helvum
Akron Zoo
Brevard Zoo
Bronx Zoo
Busch Gardens Tampa
Calgary Zoo
Cleveland Metroparks Zoo
Elmwood Park Zoo
Franklin Park Zoo
Hogle Zoo
Houston Zoo
Jacksonville Zoo
Kansas City Zoo
Lake Superior Zoo
Lincoln Park Zoo
Lowry Park Zoo
Lubee Bat Conservancy
Metro Richmond Zoo
Milwaukee County Zoo
Minnesota Zoo,
Omaha's Henry Doorly Zoo
Oregon Zoo
Point Defiance Zoo & Aquarium
Racine Zoo
Sacramento Zoo
Saint Paul's Como Zoo
Toronto Zoo
Tulsa Zoo
Egyptian fruit bat, Rousettus aegyptiacus
Blank Park Zoo
Brookfield Zoo
Cleveland Metroparks Zoo
Lincoln Park Zoo
Lubee Bat Conservancy
Memphis Zoo
Minnesota Zoo
Moody Gardens
Omaha’s Henry Doorly Zoo
Oregon Zoo
Rosamond Gifford Zoo
Timbavati Wildlife Park
Toronto Zoo
Ruwenzori long-haired fruit bat, Rousettus lanosus
Boise Zoo
Franklin Park Zoo
Lincoln Children's Zoo
Milwaukee County Zoo
Minnesota Zoo
Omaha’s Henry Doorly Zoo
Common vampire bat, Desmodus rotundus
Audubon Zoo
Buffalo Zoo
Cincinnati Zoo
Connecticut's Beardsley Zoo
Dallas World Aquarium
Denver Zoo
Louisville Zoo
Milwaukee County Zoo
North American Wildlife Park (Hershey, PA)
North Carolina Zoo
Omaha’s Henry Doorly Zoo
Philadelphia Zoo
Texas State Aquarium
Greater bulldog bat, Noctilio leporinus
Memphis Zoo
Omaha's Henry Doorly Zoo
Greater spear-nosed bat, Phyllostomus hastatus
Assiboine Park Zoo
Omaha's Henry Doorly Zoo
Peoria Zoo
Pale spear-nosed bat, Phyllostomus discolor
Miami Zoo
Pallas's long-tongued bat, Glossophaga soricina
Houston Zoo
Mesker Park Zoo
Montreal Biodome
Omaha’s Henry Doorly Zoo
Lesser long-tongued bat, Leptonycteris yerbabuenae
Fort Worth Zoo
Jamaican fruit bat, Artibeus jamaicensis
Calgary Zoo
Cameron Park Zoo
Edmonton Valley Zoo
Houston Zoo
Miami Zoo
Potawatomi Zoo
Roger Williams Park Zoo
Seba's short-tailed fruit bat, Carollia perspicillata
Akron Zoo
Audubon Zoo
Busch Gardens Tampa
Catoctin Zoo
Central Park Zoo
Dallas World Aquarium
Denver Zoo
Elmwood Park Zoo
Gladys Porter Zoo
Henry Vilas Zoo
Houston Zoo
Jacksonville Zoo
Lake Superior Zoo
Lincoln Children's Zoo
Maryland Zoo in Baltimore
Montreal Biodome
Miami Zoo
Moody Gardens
Nashville Zoo
Omaha’s Henry Doorly Zoo
Pittsburgh Zoo
Potter Park Zoo
Rolling Hills Zoo
San Antonio Zoo
Staten Island Zoo
Stone Zoo
Tulsa Zoo