diff --git a/prdoc/pr_10235.prdoc b/prdoc/pr_10235.prdoc
new file mode 100644
index 0000000000000..34df18a38b603
--- /dev/null
+++ b/prdoc/pr_10235.prdoc
@@ -0,0 +1,12 @@
+title: 'offchain-worker: Do not intialize the entire `System` again'
+doc:
+- audience: Runtime Dev
+  description: |-
+    When calling `offchain-worker` we were initializing the entire `System` again with the same block we are running on top of. However, with [the change to require strictly increasing block numbers](https://github.com/paritytech/polkadot-sdk/pull/10180) the offchain-worker was failing. This is now solved by just registering the missing digests. The rest of the changes done by `initialize` are not important for offchain workers.
+
+    The pull request ensures that we are actually testing this behavior of the offchain worker now.
+crates:
+- name: frame-executive
+  bump: patch
+- name: frame-system
+  bump: patch
diff --git a/substrate/frame/executive/src/lib.rs b/substrate/frame/executive/src/lib.rs
index 1919f890cdf15..60cde231a8c00 100644
--- a/substrate/frame/executive/src/lib.rs
+++ b/substrate/frame/executive/src/lib.rs
@@ -953,7 +953,14 @@ where
 		// OffchainWorker RuntimeApi should skip initialization.
 		let digests = header.digest().clone();
 
-		<frame_system::Pallet<System>>::initialize(header.number(), header.parent_hash(), &digests);
+		// Let's deposit all the logs we are not yet aware of. These are the logs set by the `node`.
+		let existing_digest = frame_system::Pallet::<System>::digest();
+		for digest in digests.logs().iter().filter(|d| !existing_digest.logs.contains(d)) {
+			frame_system::Pallet::<System>::deposit_log(digest.clone());
+		}
+
+		// Initialize the intra block entropy, which is maybe used by offchain workers.
+		frame_system::Pallet::<System>::initialize_intra_block_entropy(header.parent_hash());
 
 		// Frame system only inserts the parent hash into the block hashes as normally we don't know
 		// the hash for the header before. However, here we are aware of the hash and we can add it
diff --git a/substrate/frame/executive/src/tests.rs b/substrate/frame/executive/src/tests.rs
index d8d0836384054..0569f8eb52bf0 100644
--- a/substrate/frame/executive/src/tests.rs
+++ b/substrate/frame/executive/src/tests.rs
@@ -1113,7 +1113,14 @@ fn all_weights_are_recorded_correctly() {
 fn offchain_worker_works_as_expected() {
 	new_test_ext(1).execute_with(|| {
 		let parent_hash = sp_core::H256::from([69u8; 32]);
+
+		// Emulate block production before running the offchain worker.
+		System::initialize(&1, &parent_hash, &Digest::default());
+		System::finalize();
+
 		let mut digest = Digest::default();
+		// As `Seal` is added by the node after the block was build, it was not part of
+		// `System::initialize` above.
 		digest.push(DigestItem::Seal([1, 2, 3, 4], vec![5, 6, 7, 8]));
 
 		let header = Header::new(1, H256::default(), H256::default(), parent_hash, digest.clone());
diff --git a/substrate/frame/system/src/lib.rs b/substrate/frame/system/src/lib.rs
index c0729d47a6efe..9d80e6ec338d2 100644
--- a/substrate/frame/system/src/lib.rs
+++ b/substrate/frame/system/src/lib.rs
@@ -1918,8 +1918,7 @@ impl<T: Config> Pallet<T> {
 		// populate environment
 		ExecutionPhase::<T>::put(Phase::Initialization);
 		storage::unhashed::put(well_known_keys::EXTRINSIC_INDEX, &0u32);
-		let entropy = (b"frame_system::initialize", parent_hash).using_encoded(blake2_256);
-		storage::unhashed::put_raw(well_known_keys::INTRABLOCK_ENTROPY, &entropy[..]);
+		Self::initialize_intra_block_entropy(parent_hash);
 		<Number<T>>::put(number);
 		<Digest<T>>::put(digest);
 		<ParentHash<T>>::put(parent_hash);
@@ -1929,6 +1928,14 @@ impl<T: Config> Pallet<T> {
 		BlockWeight::<T>::kill();
 	}
 
+	/// Initialize [`INTRABLOCK_ENTROPY`](well_known_keys::INTRABLOCK_ENTROPY).
+	///
+	/// Normally this is called internally [`initialize`](Self::initialize) at block initiation.
+	pub fn initialize_intra_block_entropy(parent_hash: &T::Hash) {
+		let entropy = (b"frame_system::initialize", parent_hash).using_encoded(blake2_256);
+		storage::unhashed::put_raw(well_known_keys::INTRABLOCK_ENTROPY, &entropy[..]);
+	}
+
 	/// Log the entire resouce usage report up until this point.
 	///
 	/// Uses `crate::LOG_TARGET`, level `debug` and prints the weight and block length usage.
diff --git a/substrate/test-utils/runtime/src/lib.rs b/substrate/test-utils/runtime/src/lib.rs
index aace5b3e18eaa..a04b05021bb46 100644
--- a/substrate/test-utils/runtime/src/lib.rs
+++ b/substrate/test-utils/runtime/src/lib.rs
@@ -742,6 +742,7 @@ impl_runtime_apis! {
 				}.into(),
 			);
 			sp_io::offchain::submit_transaction(ext.encode()).unwrap();
+			Executive::offchain_worker(header);
 		}
 	}