diff --git a/changelog.d/2495.bugfix.md b/changelog.d/2495.bugfix.md
new file mode 100644
index 000000000..178437bc9
--- /dev/null
+++ b/changelog.d/2495.bugfix.md
@@ -0,0 +1 @@
+Fix the DNS resolver failing to start without `/etc/resolv.conf` when `dns_servers` is configured. Contributed by @eleboucher.
diff --git a/src/service/client/mod.rs b/src/service/client/mod.rs
index f258f5195..39f00b40c 100644
--- a/src/service/client/mod.rs
+++ b/src/service/client/mod.rs
@@ -338,8 +338,16 @@ fn builder_interface(
 fn get_dns_resolver(server: &Arc<Server>) -> Result<Arc<TokioResolver>> {
 	let config = &server.config;
 
-	let (system_resolver_config, mut opts) = hickory_resolver::system_conf::read_system_conf()
-		.map_err(|e| err!(error!("Failed to configure DNS resolver from system: {e}")))?;
+	let (system_resolver_config, mut opts) =
+		match hickory_resolver::system_conf::read_system_conf() {
+			| Ok(system_conf) => system_conf,
+			| Err(e) if config.dns_servers.is_empty() =>
+				return Err(err!(error!("Failed to configure DNS resolver from system: {e}"))),
+			| Err(e) => {
+				warn!("Failed to read system DNS configuration, using dns_servers: {e}");
+				Default::default()
+			},
+		};
 
 	let mut conf = ResolverConfig::from_name_servers(vec![]);
 
diff --git a/src/service/rooms/event_handler/state_at_incoming/tests.rs b/src/service/rooms/event_handler/state_at_incoming/tests.rs
index bf7e0035b..c1d4c0ef9 100644
--- a/src/service/rooms/event_handler/state_at_incoming/tests.rs
+++ b/src/service/rooms/event_handler/state_at_incoming/tests.rs
@@ -222,7 +222,8 @@ async fn test_services() -> (Arc<crate::Services>, std::path::PathBuf) {
 		"database_path": path,
 		"db_cache_capacity_mb": 16.0,
 		"rocksdb_write_buffer_capacity_mb": 4.0,
-		"allow_local_presence": false
+		"allow_local_presence": false,
+		"dns_servers": ["127.0.0.1"]
 	}))
 	.unwrap();
 	let runtime = tokio::runtime::Handle::current();