diff --git a/src/api/server.rs b/src/api/server.rs
index e4786f6d108ca..935c0b03ecaa6 100644
--- a/src/api/server.rs
+++ b/src/api/server.rs
@@ -9,6 +9,7 @@ use async_graphql::{
     Data, Request, Schema,
 };
 use async_graphql_warp::{graphql_protocol, GraphQLResponse, GraphQLWebSocket};
+use tokio::runtime::Handle;
 use tokio::sync::oneshot;
 use warp::{filters::BoxedFilter, http::Response, ws::Ws, Filter, Reply};
 
@@ -31,13 +32,13 @@ impl Server {
         config: &config::Config,
         watch_rx: topology::WatchRx,
         running: Arc<AtomicBool>,
-        runtime: &tokio::runtime::Runtime,
+        handle: &Handle,
     ) -> crate::Result<Self> {
         let routes = make_routes(config.api.playground, watch_rx, running);
 
         let (_shutdown, rx) = oneshot::channel();
         // warp uses `tokio::spawn` and so needs us to enter the runtime context.
-        let _guard = runtime.enter();
+        let _guard = handle.enter();
         let (addr, server) = warp::serve(routes)
             .try_bind_with_graceful_shutdown(
                 config.api.address.expect("No socket address"),
@@ -57,7 +58,7 @@ impl Server {
         schema::components::update_config(config);
 
         // Spawn the server in the background.
-        runtime.spawn(server);
+        handle.spawn(server);
 
         Ok(Self { _shutdown, addr })
     }
diff --git a/src/app.rs b/src/app.rs
index f306504d211c1..63d2a53bb1614 100644
--- a/src/app.rs
+++ b/src/app.rs
@@ -38,6 +38,7 @@ use crate::{
 use std::os::unix::process::ExitStatusExt;
 #[cfg(windows)]
 use std::os::windows::process::ExitStatusExt;
+use tokio::runtime::Handle;
 
 pub static WORKER_THREADS: OnceNonZeroUsize = OnceNonZeroUsize::new();
 
@@ -122,13 +123,13 @@ impl ApplicationConfig {
 
     /// Configure the API server, if applicable
     #[cfg(feature = "api")]
-    pub fn setup_api(&self, runtime: &Runtime) -> Option<api::Server> {
+    pub fn setup_api(&self, handle: &Handle) -> Option<api::Server> {
         if self.api.enabled {
             match api::Server::start(
                 self.topology.config(),
                 self.topology.watch(),
                 std::sync::Arc::clone(&self.topology.running),
-                runtime,
+                handle,
             ) {
                 Ok(api_server) => {
                     emit!(ApiStarted {
@@ -159,7 +160,8 @@ impl Application {
     }
 
     pub fn prepare_start() -> Result<(Runtime, StartedApplication), ExitCode> {
-        Self::prepare().and_then(|(runtime, app)| app.start(&runtime).map(|app| (runtime, app)))
+        Self::prepare()
+            .and_then(|(runtime, app)| app.start(runtime.handle()).map(|app| (runtime, app)))
     }
 
     pub fn prepare() -> Result<(Runtime, Self), ExitCode> {
@@ -208,13 +210,13 @@ impl Application {
         ))
     }
 
-    pub fn start(self, runtime: &Runtime) -> Result<StartedApplication, ExitCode> {
+    pub fn start(self, handle: &Handle) -> Result<StartedApplication, ExitCode> {
         // Any internal_logs sources will have grabbed a copy of the
         // early buffer by this point and set up a subscriber.
         crate::trace::stop_early_buffering();
 
         emit!(VectorStarted);
-        runtime.spawn(heartbeat::heartbeat());
+        handle.spawn(heartbeat::heartbeat());
 
         let Self {
             require_healthy,
@@ -224,7 +226,7 @@ impl Application {
 
         let topology_controller = SharedTopologyController::new(TopologyController {
             #[cfg(feature = "api")]
-            api_server: config.setup_api(runtime),
+            api_server: config.setup_api(handle),
             topology: config.topology,
             config_paths: config.config_paths.clone(),
             require_healthy,
diff --git a/src/topology/controller.rs b/src/topology/controller.rs
index 16d349fe014ed..9b64b7f050279 100644
--- a/src/topology/controller.rs
+++ b/src/topology/controller.rs
@@ -3,6 +3,7 @@ use std::sync::Arc;
 #[cfg(feature = "enterprise")]
 use futures_util::future::BoxFuture;
 use futures_util::FutureExt as _;
+
 use tokio::sync::{Mutex, MutexGuard};
 
 #[cfg(feature = "api")]
@@ -14,6 +15,7 @@ use crate::config::enterprise::{
 use crate::internal_events::{
     VectorConfigLoadError, VectorRecoveryError, VectorReloadError, VectorReloaded,
 };
+
 use crate::{config, topology::RunningTopology};
 
 #[derive(Clone, Debug)]
@@ -93,6 +95,42 @@ impl TopologyController {
             }
         }
 
+        // Start the api server or disable it, if necessary
+        #[cfg(feature = "api")]
+        if !new_config.api.enabled {
+            if let Some(server) = self.api_server.take() {
+                debug!("Dropping api server.");
+                drop(server)
+            }
+        } else if self.api_server.is_none() {
+            use crate::internal_events::ApiStarted;
+            use crate::topology::ReloadOutcome::FatalError;
+            use std::sync::atomic::AtomicBool;
+            use tokio::runtime::Handle;
+
+            debug!("Starting api server.");
+
+            self.api_server = match api::Server::start(
+                self.topology.config(),
+                self.topology.watch(),
+                Arc::<AtomicBool>::clone(&self.topology.running),
+                &Handle::current(),
+            ) {
+                Ok(api_server) => {
+                    emit!(ApiStarted {
+                        addr: new_config.api.address.unwrap(),
+                        playground: new_config.api.playground
+                    });
+
+                    Some(api_server)
+                }
+                Err(e) => {
+                    error!("An error occurred that Vector couldn't handle: {}.", e);
+                    return FatalError;
+                }
+            }
+        }
+
         match self.topology.reload_config_and_respawn(new_config).await {
             Ok(true) => {
                 #[cfg(feature = "api")]