The National First division side were faced with uncharted territory against the high-flying Polokwane, who drew 3-3 with Bidvest Wits a few days ago.
Polokwane took the lead after Mohammed Anas dribbled past the opposing goalkeeper Tshepo Ramaele for a cool tap-in on 29 minutes.
Despite receiving numerous opportunities to go further ahead, City headed into the break with a solitary lead.
At the start of the second half, Sibusiso Sikhosana took the place of Ayanda Nkili on the part of the Rise and Shine.
The visiting side wasted little time to get back in the contest through the assistance of veteran forward Edward Manqele after 56 minutes.
Veteran midfielder Jabulani Maluleke was ordered to make way for Tshepo Seabi after the midway stage in the second half.
The masses in the stands were left stunned as Manqele hit what would prove to be the winner four minutes from time.
With full-time nearing, City made an offensive change to force the game to extra time as Charlton Mashumba came on for Ndivhuwo Ravhuali, but TTM hung to claim a famous win.
Polokwane: Phali, Nkili, Mbonani, Mvalese, Ravhuhali, Seabi, Phiri, Sikhondze, Wagaba, Booi, Anas.
Subs: Ramaele, Nyadombo, Makgoka, Meso, Mokoena, Nkoana, Ndlondlo, Mabotja, Ononogbu, Manqele, Mgaga.
TTM: Ramaele, Meso, Mabotja, Mokgoga, Nyadombo, Mokoena, Mgaga, Manqele, Ononogbu, Nkoana, Ndlondlo.
Subs: Mbanjwa, Mashau, Makhubu, Bhengu, Nedzamba, Mohloding, Nkhuna.