"The president and new government are very supportive of the railways," said Nyasha Maravanyika, the railways' press relations chief, adding that talks were under way for an international consortium to fund a full-scale re-launch of the whole rail network.
"We had to re-furbish old carriages to get this service going, and it has been a huge success," Mr Maravanyika told AFP.
"The old commuter trains were suspended as the coaches and the signalling became more and more run-down."
"People know that when they are on the train, they are on their way to work," he added.
"It is an answer to their transport blues. We are here to attract commuters as kombi fares rise -- that's our job."
Mr Maravanyika says just $10 million would put the other four commuter lines back in operation.
"We hope to re-open the other Bulawayo line next and, despite all the challenges, revive Zimbabwe's railways," he said. "They were the heartbeat of the southern African rail network."
Zimbabwe's rail network -- which includes the dramatic line across the Victoria Falls into Zambia -- was built under British colonial rule, and at its peak in the 1990s had 600 locomotives and 3,000 passenger carriages.
Today it has less than 100 locomotives and a few hundred carriages, running a threadbare schedule between major cities, and a much-reduced freight service carrying sugar, chrome and quarried stone.
The main line between Harare and Bulawayo -- opened in 1907 -- was once electrified, but vandalism stripped it of its copper cables, signalling system and track motors.
Today, diesel-powered trains on the line are often hugely delayed and drivers are often forced to communicate using text and WhatsApp messages, Mr Maravanyika said.
On the Bulawayo commuter train, some windows on older carriages are even still marked "RR" for "Rhodesian Railways" -- Zimbabwe's name before independence in 1980.
Rattling along on her return journey home, Ashley Sinda, 40, was weary after a long day working as a cleaner at a pharmaceutical company.
"I live 300 metres (990 feet) from the last stop, so it is easy for me," said the single mother of two, sitting among nurses, teachers, office workers staring at mobile phones and labourers who swilled cheap local beer.
"It is impossible to afford the kombis, even if they are faster," she said. "I am glad of this train, it is a good thing for us."