He spoke via a live video link from the Museum of the American Revolution in Philadelphia — a venue chosen to underscore the gravity of the choice facing voters in November.
“This administration has shown it will tear our democracy down if that’s what it takes to win,” Mr Obama said.
Former US presidents have in the past shied away from criticising the incumbent. But in a scathing speech, Mr Obama said Mr Trump had “no interest in putting in the work” required of a president.
“Donald Trump hasn’t grown into the job because he can’t. And the consequences of that failure are severe — 170,000 Americans dead; millions of jobs gone.”
Mr Trump appeared to be watching Mr Obama’s speech live and tweeted in all-caps as the former president was speaking: “Why did he refuse to endorse slow Joe until it was all over . . . why did he try to get him not to run?”
Mr Obama was followed by Kamala Harris, who accepted the Democratic nomination for vice-president in an uplifting speech pointing to the historic nature of her candidacy while also attacking Mr Trump for the “lives and livelihoods” lost during the pandemic.
Ms Harris became the first woman of colour to join a major party ticket when Joe Biden picked her as his running mate and she used her address to lament the impact of coronavirus on minority communities.
She said: “[Covid] is not an equal opportunity offender. Black, Latino and indigenous people are suffering and dying disproportionately . . . Let’s be clear — there is no vaccine for racism.”
Mr Obama was originally scheduled to cap the night, but the running order of the virtual convention was switched at the last minute in a symbolic move that was taken as a passing of the torch from the 44th president to Ms Harris.
Although Ms Harris did attack Mr Trump — accusing him of turning “our tragedies into political weapons” — she devoted most of her speech to fleshing out a positive vision of an America “where all are welcome, no matter what we look like”.
Ms Harris drew on her personal story as the daughter of an Indian mother and Jamaican father and credited her appearance on the ticket “to the dedication of generations before me”.
She also spoke of the importance of her family, including her husband “who I met on a blind date”, their children, and her “chitthis” — the Tamil word for aunt.
Ms Harris was preceded by several of the party’s best-known women, including Hillary Clinton, the party’s 2016 presidential candidate and Nancy Pelosi, House speaker. Mr Biden, who was formally nominated as the party’s presidential candidate on Tuesday, will speak on Thursday evening.
The themes of the third night of the convention included several issues of particular concern to the party’s progressive wing: gun control, climate change and immigration reform.
Speaking from her home in New York, Mrs Clinton used her stinging defeat in 2016 to urge potential Democratic voters to “vote like our livelihoods are on the line”.
“Remember, Joe and Kamala can win 3m more votes and still lose — take it from me,” she said.
Mrs Clinton said that voters had failed to appreciate “how dangerous” a Trump presidency would be. “For four years, people have said to me . . . ‘I wish I could go back and do it over’. Or, worse, ‘I should have voted’. Well, this can’t be another woulda, coulda, shoulda election.”
Mrs Pelosi also made the case against Mr Trump. “I’ve seen first-hand Donald Trump’s disrespect for facts, for working families, and for women in particular — disrespect written into his policies toward our health and our rights, not just his conduct,” she said.