The identification cards — set to be issued in December — will function like any Ventra card, officials said.
The cards have been touted by Mayor Rahm Emanuel and City Clerk Anna Valencia as a way to help anyone who cannot get a government-issued identification card to access city services and other benefits.
"An individual's background should never be a barrier to participating in the economic, social or cultural vibrancy of Chicago," Emanuel said. "Today we are a step closer to ensuring all residents — whether immigrant, homeless or returning citizen — have the identification they need to access the resources they deserve."
The cards are designed to bring Chicago's undocumented immigrants, homeless residents and individuals with a criminal record "out of the shadows," Emanuel has said.
The Chicago Transit Board approved the agreement to add Ventra to the municipal identification cards at its meeting Wednesday afternoon.
The Municipal ID cards will be printed on blank Ventra cards, and the city will reimburse the CTA for the costs of the cards, officials said.
The city has spent $1 million developing the cards, which were the subject of an emotional debate among aldermen in April.
Valencia has promised to ensure that the information provided by undocumented immigrants to city officials would not be used by members of President Donald Trump's administration to deport people here without documentation.
The city will not keep applicants' addresses and phone numbers on record nor will they keep copies of any documents, Valencia has said.
City officials have not determined what documents applicants for the identification card will need to present beyond their names and dates of birth. Officials also have not decided whether there will be a fee for the card, but the proposal introduced Wednesday would allow one to be charged.
Applicants would be able to self-designate their gender in response to concerns from members of the transgender community, and each card would have a unique number as well as security features to prevent fraud, Valencia said.