Around four million voters in the former German industrial heartland are expected to cast their ballots, six months after a similar initiative was successfully put to a vote in Munich.
The Rhine/Ruhr region -- which includes the cities of Cologne, Duesseldorf and Dortmund -- is among four bids alongside Berlin, Munich and Hamburg.
Amid a growing backlash against the impact of major events like the Olympics, authorities are hoping for positive results to illustrate a groundswell of public support.
The German Olympic Committee (DOSB) will consider the four bids before submitting one to the International Olympic Committee in late September.
Unlike the usual process, where a country or city puts in a bid for a specific edition of the games, the DOSB is keeping its options open regarding the target year in the hope of a greater shot at success.
With Olympic Games often shifting continents from edition to edition, Asia is considered to be a frontrunner for the 2036 edition.
Berlin's bid included potentially hosting the games 100 years after the 1936 edition under Nazi rule.
Just three years before the start of the Second World War, then German Chancellor Adolf Hitler tried to use the 1936 games for propaganda purposes.
Berlin mayor Kai Wegner said the anniversary could be used to show "that we no longer stand for dictatorship, exclusion, and mass violence, but that Berlin is now a cosmopolitan, international metropolis, a colourful, diverse city".
Not everyone is convinced, however.
German President Frank-Walter Steinmeier said he considers the date "historically problematic," while indicating he prefers a bid for 2040 or 2044.
The last summer Olympics on German soil took place in 1972, in Munich, then part of West Germany.
That edition was also shrouded in controversy and tragedy, when Palestinian militants infiltrated the Olympic Village and killed 11 members of the Israeli Olympic team.
A 'significant advantage'
After Munich and Rhine/Ruhr, Hamburg will hold a vote on May 31.
While the results of the referenda will not be the only factor under consideration for the DOSB, the public consultation has been done amid growing resistance to hosting the Olympics from local groups.
Images of decaying Olympic venues, including in recent host cities Athens and Rio de Janeiro, alongside spiralling costs have drawn public ire.
Rather than images of shiny new facilities, modern bids have sought to emphasise low public costs through the re-use of existing infrastructure.
While democratic, the public consultation strategy does not come without risks.
In 2015, voters in Hamburg previously rejected a proposal to host the 2024 Summer Olympics, with Munich voters doing the same for the 2022 Winter Olympics two years before.
Jean-Loup Chappelet, an Olympic expert from the University of Lausanne, told AFP holding a referendum is "a good idea" in the current climate.
Chappelet said the Paris 2024 Olympics, which largely relied on existing infrastructure, "showed it was possible to host the games without going into too much debt."
"It's not mandated by the IOC, but it's a significant advantage," Chappelet said of hosting a referendum.
"It's very important, even more so today than before, because there have been dozens of negative referenda."
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