diff --git a/bridges/relays/lib-substrate-relay/src/messages_source.rs b/bridges/relays/lib-substrate-relay/src/messages_source.rs
index 8d2ac5874fe6..a151af8ee827 100644
--- a/bridges/relays/lib-substrate-relay/src/messages_source.rs
+++ b/bridges/relays/lib-substrate-relay/src/messages_source.rs
@@ -129,8 +129,22 @@ impl<P: SubstrateMessageLane> RelayClient for SubstrateMessagesSource<P> {
 	type Error = SubstrateError;
 
 	async fn reconnect(&mut self) -> Result<(), SubstrateError> {
+		// since the client calls RPC methods on both sides, we need to reconnect both
 		self.source_client.reconnect().await?;
-		self.target_client.reconnect().await
+		self.target_client.reconnect().await?;
+
+		// call reconnect on on-demand headers relay, because we may use different chains there
+		// and the error that has lead to reconnect may have came from those other chains
+		// (see `require_target_header_on_source`)
+		//
+		// this may lead to multiple reconnects to the same node during the same call and it
+		// needs to be addressed in the future
+		// TODO: https://github.com/paritytech/parity-bridges-common/issues/1928
+		if let Some(ref mut target_to_source_headers_relay) = self.target_to_source_headers_relay {
+			target_to_source_headers_relay.reconnect().await?;
+		}
+
+		Ok(())
 	}
 }
 
diff --git a/bridges/relays/lib-substrate-relay/src/messages_target.rs b/bridges/relays/lib-substrate-relay/src/messages_target.rs
index 75119a1de976..7b0d9d63fb78 100644
--- a/bridges/relays/lib-substrate-relay/src/messages_target.rs
+++ b/bridges/relays/lib-substrate-relay/src/messages_target.rs
@@ -123,8 +123,22 @@ impl<P: SubstrateMessageLane> RelayClient for SubstrateMessagesTarget<P> {
 	type Error = SubstrateError;
 
 	async fn reconnect(&mut self) -> Result<(), SubstrateError> {
+		// since the client calls RPC methods on both sides, we need to reconnect both
 		self.target_client.reconnect().await?;
-		self.source_client.reconnect().await
+		self.source_client.reconnect().await?;
+
+		// call reconnect on on-demand headers relay, because we may use different chains there
+		// and the error that has lead to reconnect may have came from those other chains
+		// (see `require_source_header_on_target`)
+		//
+		// this may lead to multiple reconnects to the same node during the same call and it
+		// needs to be addressed in the future
+		// TODO: https://github.com/paritytech/parity-bridges-common/issues/1928
+		if let Some(ref mut source_to_target_headers_relay) = self.source_to_target_headers_relay {
+			source_to_target_headers_relay.reconnect().await?;
+		}
+
+		Ok(())
 	}
 }
 
diff --git a/bridges/relays/lib-substrate-relay/src/on_demand/headers.rs b/bridges/relays/lib-substrate-relay/src/on_demand/headers.rs
index 75b402aff873..090019f087f6 100644
--- a/bridges/relays/lib-substrate-relay/src/on_demand/headers.rs
+++ b/bridges/relays/lib-substrate-relay/src/on_demand/headers.rs
@@ -60,6 +60,8 @@ pub struct OnDemandHeadersRelay<P: SubstrateFinalitySyncPipeline> {
 	required_header_number: RequiredHeaderNumberRef<P::SourceChain>,
 	/// Client of the source chain.
 	source_client: Client<P::SourceChain>,
+	/// Client of the target chain.
+	target_client: Client<P::TargetChain>,
 }
 
 impl<P: SubstrateFinalitySyncPipeline> OnDemandHeadersRelay<P> {
@@ -83,6 +85,7 @@ impl<P: SubstrateFinalitySyncPipeline> OnDemandHeadersRelay<P> {
 			relay_task_name: on_demand_headers_relay_name::<P::SourceChain, P::TargetChain>(),
 			required_header_number: required_header_number.clone(),
 			source_client: source_client.clone(),
+			target_client: target_client.clone(),
 		};
 		async_std::task::spawn(async move {
 			background_task::<P>(
@@ -104,6 +107,13 @@ impl<P: SubstrateFinalitySyncPipeline> OnDemandHeadersRelay<P> {
 impl<P: SubstrateFinalitySyncPipeline> OnDemandRelay<P::SourceChain, P::TargetChain>
 	for OnDemandHeadersRelay<P>
 {
+	async fn reconnect(&self) -> Result<(), SubstrateError> {
+		// using clone is fine here (to avoid mut requirement), because clone on Client clones
+		// internal references
+		self.source_client.clone().reconnect().await?;
+		self.target_client.clone().reconnect().await
+	}
+
 	async fn require_more_headers(&self, required_header: BlockNumberOf<P::SourceChain>) {
 		let mut required_header_number = self.required_header_number.lock().await;
 		if required_header > *required_header_number {
diff --git a/bridges/relays/lib-substrate-relay/src/on_demand/mod.rs b/bridges/relays/lib-substrate-relay/src/on_demand/mod.rs
index eca7d20163d2..00bb33d67409 100644
--- a/bridges/relays/lib-substrate-relay/src/on_demand/mod.rs
+++ b/bridges/relays/lib-substrate-relay/src/on_demand/mod.rs
@@ -26,6 +26,9 @@ pub mod parachains;
 /// On-demand headers relay that is relaying finalizing headers only when requested.
 #[async_trait]
 pub trait OnDemandRelay<SourceChain: Chain, TargetChain: Chain>: Send + Sync {
+	/// Reconnect to source and target nodes.
+	async fn reconnect(&self) -> Result<(), SubstrateError>;
+
 	/// Ask relay to relay source header with given number  to the target chain.
 	///
 	/// Depending on implementation, on-demand relay may also relay `required_header` ancestors
diff --git a/bridges/relays/lib-substrate-relay/src/on_demand/parachains.rs b/bridges/relays/lib-substrate-relay/src/on_demand/parachains.rs
index 672530de3a58..4c205770d4ac 100644
--- a/bridges/relays/lib-substrate-relay/src/on_demand/parachains.rs
+++ b/bridges/relays/lib-substrate-relay/src/on_demand/parachains.rs
@@ -119,6 +119,15 @@ impl<P: SubstrateParachainsPipeline> OnDemandRelay<P::SourceParachain, P::Target
 where
 	P::SourceParachain: Chain<Hash = ParaHash>,
 {
+	async fn reconnect(&self) -> Result<(), SubstrateError> {
+		// using clone is fine here (to avoid mut requirement), because clone on Client clones
+		// internal references
+		self.source_relay_client.clone().reconnect().await?;
+		self.target_client.clone().reconnect().await?;
+		// we'll probably need to reconnect relay chain relayer clients also
+		self.on_demand_source_relay_to_target_headers.reconnect().await
+	}
+
 	async fn require_more_headers(&self, required_header: BlockNumberOf<P::SourceParachain>) {
 		if let Err(e) = self.required_header_number_sender.send(required_header).await {
 			log::trace!(