Jews refer to the site as the Temple Mount, referencing two temples that were said to have stood there in antiquity. Al-Aqsa is at the heart of the Israeli-Palestinian conflict, falling within Israeli-annexed east Jerusalem, but administered by the Waqf Islamic affairs council.
The Waqf called the Tuesday ruling by Jerusalem Magistrates' Court judge Billha Yahalom an illegitimate "provocation," while Palestinian prime minister Mohammed Shtayyeh warned Israel against any moves to enforce it.
Even Israeli police have appealed the decision, which came in response to a petition by an Israeli rabbi, Aryeh Lippo, who on September 29 was slapped with a two-week ban from the plaza after praying there.
The Waqf reluctantly grants Jews limited access to the site at certain hours, but the Jewish presence at the Al-Aqsa has long been a rallying cry across the Muslim world.
Before Israel's 1948 creation, riots during the British mandate of Palestine in 1929 were linked to the possibility of Jewish prayer there.
In May this year, clashes over possible evictions in a nearby Palestinian neighbourhood spread to the mosque compound, sparking an Israeli crackdown that escalated into an 11-day assault on the Palestinians in the Gaza Strip.
- 'Whispered' –
No Israeli law prohibits Jewish prayer at the site, the third holiest to Islam.
But since 1967, the year Israel captured east Jerusalem including the Old City in the Six Day War, Israeli authorities have enforced a ban on Jewish prayer to prevent tensions.
Judge Yahalom's legal ruling was narrowly focused on overturning Lippo's ban from the plaza.
But commenting on his conduct, she wrote: "The appellant stood in the corner with a friend or two, there was no crowd around him, his prayer was quiet, whispered."
"I have not found that the religious acts carried out by the appellant were externalised and visible," she ruled, determining that such prayer did "not violate police instructions," and cancelling his ban from the site.
In appealing the ruling, police said Lippo engaged in "improper conduct in the public sphere."
- 'Not absolute' –
Mainstream rabbinical authorities oppose Jewish prayer on the Temple Mount, with Jewish worship centred at the Western Wall plaza below.
In a ruling earlier this year on a petition demanding Temple Mount prayer rights for Jews, Israel's Supreme Court found that, "every Jew has the right to pray on the Temple Mount, as part of the freedom of religion and expression."
"At the same time, these rights are not absolute, and can be limited to take into account the public interest."
Muslim leaders reacted to the Jerusalem court ruling with unanimous condemnation.
"These prayers constitute provocations and a violation of the sanctity of Al-Aqsa," mosque director Sheikh Omar al-Kiswani told AFP.
"This decision also has no legitimacy because we do not recognise Israeli law on Al-Aqsa," he said.
The Saudi Arabia-based Organisation of Islamic Cooperation strongly condemned "the decision of the so-called Israeli 'Jerusalem Court.'"
Some Jewish leaders were meanwhile underwhelmed by the impact of the decision.
Long-time activist for Jewish Temple Mount prayer Arnon Segal stressed that despite Yahalom's sentiment, "the simple truth is that (Jewish) prayer is prohibited on the Temple Mount."
"There's no change in policy," he wrote on Twitter, noting that on Thursday police had detained a Jewish man for silent prayer, and accusing the state of "trampling" the rights of those prevented from praying.
Segal further told AFP that not only was Yahalom's ruling not a precedent, it would likely harm his cause.
"The harsh Palestinian reaction to the very weak ruling will deter the justice system and the state from even enabling quiet prayers," he said.
On Thursday pensioner Naseef Ismael visited Al-Aqsa and said he disagreed with allowing Jews to pray there.
"This is a gift from God to Muslims, and there is no right for any person other than Muslims to do so," he told AFP.