Lovemore Moyo of the Movement for Democratic Change got 110 votes in the 210 member assembly, giving the opposition one of the most powerful positions in Zimbabwean politics for the first time since 1980.
Moyo comfortably beat a candidate put up by a breakaway opposition faction and backed by Mugabe's ZANU-PF party, a sign the veteran leader might be unable to use parliament to force his way in deadlocked power-sharing talks.
Opposition lawmakers broke into song after the result, mocking Mugabe's ruling ZANU-PF party as a dying party.
Negotiations between ZANU-PF and Morgan Tsvangirai's MDC have stalled over what the opposition says is Mugabe's refusal to give up executive power after 28 years in office.
The deadlock, in spite of strong regional and international pressure for a deal, has dampened hopes of an agreement that could end the political crisis and revive the broken economy.
In Zimbabwe's hung parliament, the speaker will be able to take charge of controversial debates if there is no power-sharing deal.
The speaker can also act as president in the absence of the vice president or Senate president.
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