Lawyers representing the Dutch government told the European Court of Human Rights in the French city of Strasbourg that Russia had effective control over rebel forces in eastern Ukraine when Malaysia Airlines flight MH17 was shot down on July 17, 2014.
The preliminary hearing into whether the Ukraine and Dutch cases against Russia are admissible opened amid soaring tensions between Russia and NATO over fears of conflict in Ukraine.
Ukrainian Justice Minister Denys Maliuska told the court that the events in eastern Ukraine and Crimea in 2014 foreshadowed the current crisis.
He told the court his country faces "a consistent or long-term policy of the Russian Federation aimed at bending Ukraine to the Russian interests and swaying it away from its path towards Western values and civilisation. This policy continues up until now".
An international investigation concluded that a Buk missile transported from a Russian military base into Ukraine brought down the Boeing 777 that was heading from Amsterdam to Kuala Lumpur.
The missile launch system was then driven back to Russia, the investigation concluded.
At the time, pro-Russian separatists were battling Ukrainian forces in the country's east.
Dutch lawyer Babette Koopman said the Dutch government had concluded that the missile launch system "was provided by Russia with a crew to the separatists. The Buk missile was launched from an area under the effective control of Russia and by, or at least with the assistance of, Russian state agents".
Koopman told judges that relatives of the plane's dead are still waiting for an admission of responsibility and the fact that none has been made "has added and continues to add to the already tremendous grief of the next of kin".
Maliuska went to the court to personally argue his government's case.
He told judges that after Russia's annexation of Crimea in 2014, Russia used "this same travelling circus of professional separatists" in eastern Ukraine.
Russia denies any involvement and its lawyer Mikhail Vinogradov urged the court to declare the cases inadmissible.
If the Dutch and Ukrainian cases are deemed admissible by the court's judges, they will likely take years to reach a conclusion.
Relatives of some of the victims were in court on Wednesday.
Before the hearing, they held up a banner outside that read "Waiting for answers and accountability" printed over the flight number MH17.
Three Russians and a Ukrainian are on trial in the Netherlands for their alleged roles in the downing in a criminal case that is separate from the hearings in Strasbourg.
None of the four have appeared for trial in the Netherlands.
In a statement, Dutch Foreign Minister Wopke Hoekstra called Wednesday's hearing "an important step in the Netherlands' pursuit of justice for the victims and their next of kin".
All 298 people onboard MH17 were killed, including 38 from Australia and many from the Netherlands.
