diff --git a/crates/misc/component-async-tests/tests/scenario/backpressure.rs b/crates/misc/component-async-tests/tests/scenario/backpressure.rs
index 21f18cdf2723..92bd66b4a97b 100644
--- a/crates/misc/component-async-tests/tests/scenario/backpressure.rs
+++ b/crates/misc/component-async-tests/tests/scenario/backpressure.rs
@@ -1,13 +1,127 @@
-use wasmtime::Result;
+use component_async_tests::Ctx;
+use std::{
+    env, future,
+    pin::Pin,
+    task::{Context, Poll},
+    time::Duration,
+};
+use wasmtime::{
+    Engine, Result, Store,
+    component::{Linker, ResourceTable},
+};
+use wasmtime_wasi::WasiCtxBuilder;
 
-use super::util::test_run;
+use super::util::{config, make_component, test_run};
 
-// No-op function; we only test this by composing it in `async_backpressure_caller`
-#[allow(
-    dead_code,
-    reason = "here only to make the `assert_test_exists` macro happy"
-)]
-pub fn async_backpressure_callee() {}
+mod callee {
+    wasmtime::component::bindgen!({
+        path: "wit",
+        world: "backpressure-callee",
+        exports: { default: async | store },
+    });
+}
+
+#[tokio::test]
+pub async fn async_backpressure_callee() -> Result<()> {
+    let mut config = config();
+    // As of this writing, miri/pulley/epochs is a problematic combination, so
+    // we don't test it.
+    if env::var_os("MIRI_TEST_CWASM_DIR").is_none() {
+        config.epoch_interruption(true);
+    }
+
+    let engine = Engine::new(&config)?;
+    let component = make_component(
+        &engine,
+        &[test_programs_artifacts::ASYNC_BACKPRESSURE_CALLEE_COMPONENT],
+    )
+    .await?;
+    let mut linker = Linker::new(&engine);
+    wasmtime_wasi::p2::add_to_linker_async(&mut linker)?;
+
+    let mut store = Store::new(
+        &engine,
+        Ctx {
+            wasi: WasiCtxBuilder::new().inherit_stdio().build(),
+            table: ResourceTable::default(),
+            continue_: false,
+        },
+    );
+
+    if env::var_os("MIRI_TEST_CWASM_DIR").is_none() {
+        store.set_epoch_deadline(1);
+
+        std::thread::spawn(move || {
+            std::thread::sleep(Duration::from_secs(10));
+            engine.increment_epoch();
+        });
+    }
+
+    let guest =
+        callee::BackpressureCallee::instantiate_async(&mut store, &component, &linker).await?;
+
+    store
+        .run_concurrent(async |accessor| {
+            guest
+                .local_local_backpressure()
+                .call_inc_then_later_dec_backpressure(accessor)
+                .await?;
+
+            let mut instance = Some(Box::pin(
+                guest
+                    .local_local_run()
+                    .func_run()
+                    .func()
+                    .ready_for_concurrent_call(accessor),
+            ));
+
+            let mut a = Some(Box::pin(guest.local_local_run().call_run(accessor)));
+            let mut b = Some(Box::pin(guest.local_local_run().call_run(accessor)));
+            let mut c = Some(Box::pin(guest.local_local_run().call_run(accessor)));
+
+            let mut backpressure_is_set = true;
+            future::poll_fn(move |cx| {
+                let instance_ready = is_ready(cx, &mut instance);
+                let a_ready = is_ready(cx, &mut a);
+                let b_ready = is_ready(cx, &mut b);
+                let c_ready = is_ready(cx, &mut c);
+
+                if backpressure_is_set {
+                    assert!(!instance_ready);
+                    assert!(!a_ready);
+                    assert!(!b_ready);
+                    assert!(!c_ready);
+
+                    backpressure_is_set = false;
+
+                    Poll::Pending
+                } else if instance_ready && a_ready && b_ready && c_ready {
+                    Poll::Ready(())
+                } else {
+                    Poll::Pending
+                }
+            })
+            .await;
+
+            wasmtime::error::Ok(())
+        })
+        .await??;
+
+    Ok(())
+}
+
+fn is_ready(cx: &mut Context, fut: &mut Option<Pin<Box<impl Future>>>) -> bool {
+    if let Some(v) = fut.as_mut() {
+        if v.as_mut().poll(cx).is_ready() {
+            *fut = None;
+            true
+        } else {
+            false
+        }
+    } else {
+        true
+    }
+}
 
 #[tokio::test]
 pub async fn async_backpressure_caller() -> Result<()> {
diff --git a/crates/misc/component-async-tests/wit/test.wit b/crates/misc/component-async-tests/wit/test.wit
index 84efb8ec40a0..59eae0d05deb 100644
--- a/crates/misc/component-async-tests/wit/test.wit
+++ b/crates/misc/component-async-tests/wit/test.wit
@@ -63,6 +63,7 @@ interface backpressure {
   set-backpressure: func(enabled: bool);
   inc-backpressure: func();
   dec-backpressure: func();
+  inc-then-later-dec-backpressure: async func();
 }
 
 interface transmit {
diff --git a/crates/test-programs/src/bin/async_backpressure_callee.rs b/crates/test-programs/src/bin/async_backpressure_callee.rs
index 7f89a67d77fa..ec1fef7f0529 100644
--- a/crates/test-programs/src/bin/async_backpressure_callee.rs
+++ b/crates/test-programs/src/bin/async_backpressure_callee.rs
@@ -32,6 +32,16 @@ impl Backpressure for Component {
     fn dec_backpressure() {
         wit_bindgen::backpressure_dec();
     }
+    async fn inc_then_later_dec_backpressure() {
+        wit_bindgen::backpressure_inc();
+
+        wit_bindgen::spawn_local(async {
+            for _ in 0..10 {
+                wit_bindgen::yield_async().await;
+            }
+            wit_bindgen::backpressure_dec();
+        });
+    }
 }
 
 // Unused function; required since this file is built as a `bin`:
diff --git a/crates/test-programs/src/bin/async_cancel_callee.rs b/crates/test-programs/src/bin/async_cancel_callee.rs
index 2ee686dec974..b92410843cf5 100644
--- a/crates/test-programs/src/bin/async_cancel_callee.rs
+++ b/crates/test-programs/src/bin/async_cancel_callee.rs
@@ -97,6 +97,16 @@ unsafe extern "C" fn export_dec_backpressure() {
     wit_bindgen::backpressure_dec();
 }
 
+#[unsafe(export_name = "[async-lift]local:local/backpressure#inc-then-later-dec-backpressure")]
+unsafe extern "C" fn export_inc_then_later_dec_backpressure() -> u32 {
+    todo!()
+}
+
+#[unsafe(export_name = "[callback][async-lift]local:local/backpressure#inc-then-later-dec-backpressure")]
+unsafe extern "C" fn callback_inc_then_later_dec_backpressure(_: u32, _: u32, _: u32) -> u32 {
+    todo!()
+}
+
 #[unsafe(export_name = "local:local/yield#yield-times")]
 unsafe extern "C" fn export_yield_yield_times(times: u64) {
     unsafe {
diff --git a/crates/wasi-http/src/handler.rs b/crates/wasi-http/src/handler.rs
index 2dc49ab90766..69f8fa7bf61f 100644
--- a/crates/wasi-http/src/handler.rs
+++ b/crates/wasi-http/src/handler.rs
@@ -31,7 +31,7 @@ use std::sync::{
 use std::task::{Context, Poll};
 use std::time::Instant;
 use tokio::sync::Notify;
-use wasmtime::component::{Accessor, GuestTaskId, Resource, TypedFuncCallConcurrent};
+use wasmtime::component::{Accessor, GuestTaskId, HasData, Resource, TypedFuncCallConcurrent};
 #[cfg(feature = "p2")]
 use wasmtime::error::Context as _;
 use wasmtime::{AsContextMut, Result, Store, StoreContextMut, format_err};
@@ -793,6 +793,7 @@ where
                     Some((pair, queue))
                 }
             ));
+            let mut ready = pin!(when_ready(accessor, proxy));
             future::poll_fn(|cx| {
                 loop {
                     // First, and crucially first, poll `futures`. This way
@@ -839,6 +840,13 @@ where
                         Poll::Ready(None) | Poll::Pending => {}
                     }
 
+                    ready.set(when_ready(accessor, proxy));
+                    let is_ready = match ready.as_mut().poll(cx) {
+                        Poll::Ready(Ok(())) => true,
+                        Poll::Ready(Err(error)) => break Poll::Ready(Err(error)),
+                        Poll::Pending => false,
+                    };
+
                     // At this point `futures` is either empty or it's `Pending`
                     // meaning nothing is ready. Note that `Pending` here
                     // doesn't necessarily mean all tasks are blocked on I/O.
@@ -850,6 +858,7 @@ where
                     // at all or all our tasks really are blocked on I/O.
                     self.set_available(
                         may_accept
+                            && is_ready
                             && match dropper
                                 .state
                                 .should_accept_request(futures.len(), reuse_count)
@@ -905,7 +914,7 @@ where
                     // if we're not actually capable of accepting any more work,
                     // then we're completely done and it's time to exit this
                     // worker.
-                    if !may_accept {
+                    if !(may_accept && is_ready) {
                         break Poll::Ready(Ok(()));
                     }
 
@@ -1401,3 +1410,26 @@ impl<'a, T: Send> Prepared<'a, T> {
         }
     }
 }
+
+async fn when_ready<T, D: HasData>(accessor: &Accessor<T, D>, proxy: &Proxy) -> Result<()> {
+    match proxy {
+        #[cfg(feature = "p3")]
+        Proxy::P3(guest) => {
+            guest
+                .wasi_http_handler()
+                .func_handle()
+                .func()
+                .ready_for_concurrent_call(accessor)
+                .await
+        }
+        #[cfg(feature = "p2")]
+        Proxy::P2(guest) => {
+            guest
+                .wasi_http_incoming_handler()
+                .func_handle()
+                .func()
+                .ready_for_concurrent_call(accessor)
+                .await
+        }
+    }
+}
diff --git a/crates/wasmtime/src/runtime/component/concurrent.rs b/crates/wasmtime/src/runtime/component/concurrent.rs
index 5ec4de15bb15..d858f61ccf30 100644
--- a/crates/wasmtime/src/runtime/component/concurrent.rs
+++ b/crates/wasmtime/src/runtime/component/concurrent.rs
@@ -1843,6 +1843,9 @@ impl StoreOpaque {
     /// Iterate over `InstanceState::pending`, moving any ready items into the
     /// "high priority" work item queue.
     ///
+    /// Also, wake any wakers interested in the transition from not ready to
+    /// ready.
+    ///
     /// See `GuestCall::is_ready` for details.
     fn partition_pending(&mut self, instance: RuntimeInstance) -> Result<()> {
         for (thread, kind) in
@@ -1860,6 +1863,20 @@ impl StoreOpaque {
             }
         }
 
+        for waker in self
+            .instance_state(instance)
+            .concurrent_state()
+            .wakers
+            .get_mut()
+            .iter_mut()
+        {
+            if let Some(waker) = waker.downcast_ref::<Waker>() {
+                waker.wake_by_ref();
+            } else {
+                bail_bug!("`ConcurrentInstanceState::wakers` should contain only `Waker`s");
+            }
+        }
+
         Ok(())
     }
 
@@ -4989,6 +5006,7 @@ pub struct ConcurrentInstanceState {
     /// Pending calls for this instance which require `Self::backpressure` to be
     /// `true` and/or `Self::do_not_enter` to be false before they can proceed.
     pending: BTreeMap<QualifiedThreadId, GuestCallKind>,
+    wakers: AlwaysMut<ResourceTable>,
 }
 
 impl ConcurrentInstanceState {
@@ -5702,3 +5720,69 @@ fn queue_call0<T: 'static>(
         )
     }
 }
+
+pub(crate) struct ReadyToCall<'a, T: 'static, D: HasData + ?Sized> {
+    accessor: &'a Accessor<T, D>,
+    func: Func,
+    waker_key: Option<Resource<Waker>>,
+}
+
+impl<T, D: HasData + ?Sized> Future for ReadyToCall<'_, T, D> {
+    type Output = Result<()>;
+
+    fn poll(mut self: Pin<&mut Self>, cx: &mut Context<'_>) -> Poll<Self::Output> {
+        self.accessor.with(|mut store| {
+            let store = store.as_context_mut();
+            let (_, _, _, raw_options) = self.func.abi_info(store.0);
+            let instance = self.func.instance().runtime_instance(raw_options.instance);
+            let state = store.0.instance_state(instance).concurrent_state();
+            if state.backpressure == 0 {
+                Poll::Ready(Ok(()))
+            } else {
+                let waker = cx.waker().clone();
+                if let Some(key) = &self.waker_key {
+                    *state.wakers.get_mut().get_mut(key).unwrap() = waker;
+                } else {
+                    self.waker_key = Some(
+                        state
+                            .wakers
+                            .get_mut()
+                            .push(waker)
+                            .map_err(crate::Error::from)?,
+                    );
+                }
+                Poll::Pending
+            }
+        })
+    }
+}
+
+impl<T, D: HasData + ?Sized> Drop for ReadyToCall<'_, T, D> {
+    fn drop(&mut self) {
+        if let Some(key) = self.waker_key.take() {
+            self.accessor.with(|mut store| {
+                let store = store.as_context_mut();
+                let (_, _, _, raw_options) = self.func.abi_info(store.0);
+                let instance = self.func.instance().runtime_instance(raw_options.instance);
+                _ = store
+                    .0
+                    .instance_state(instance)
+                    .concurrent_state()
+                    .wakers
+                    .get_mut()
+                    .delete(key);
+            });
+        }
+    }
+}
+
+pub(crate) fn ready_to_call<'a, T, D: HasData + ?Sized>(
+    accessor: &'a Accessor<T, D>,
+    func: Func,
+) -> ReadyToCall<'a, T, D> {
+    ReadyToCall {
+        accessor,
+        func,
+        waker_key: None,
+    }
+}
diff --git a/crates/wasmtime/src/runtime/component/concurrent/func.rs b/crates/wasmtime/src/runtime/component/concurrent/func.rs
index 371bb8e621e9..365c0c7a5e93 100644
--- a/crates/wasmtime/src/runtime/component/concurrent/func.rs
+++ b/crates/wasmtime/src/runtime/component/concurrent/func.rs
@@ -163,6 +163,17 @@ impl Func {
         Ok(())
     }
 
+    /// Returns a future which will resolve once the component instance
+    /// corresponding to this function is ready to run a concurrent call without
+    /// queuing it (i.e. does not have backpressure enabled and does not have a
+    /// sync call in progress).
+    pub async fn ready_for_concurrent_call<T: 'static>(
+        self,
+        accessor: impl AsAccessor<Data = T>,
+    ) -> Result<()> {
+        concurrent::ready_to_call(accessor.as_accessor(), self).await
+    }
+
     /// Calls `concurrent::prepare_call` with monomorphized functions for
     /// lowering the parameters and lifting the result.
     fn prepare_call_dynamic<'a, T: Send + 'static>(