diff --git a/crates/misc/component-async-tests/tests/scenario/backpressure.rs b/crates/misc/component-async-tests/tests/scenario/backpressure.rs
index 21f18cdf2723..782706011b31 100644
--- a/crates/misc/component-async-tests/tests/scenario/backpressure.rs
+++ b/crates/misc/component-async-tests/tests/scenario/backpressure.rs
@@ -1,13 +1,121 @@
-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 func = *guest.local_local_run().func_run().func();
+
+            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 = accessor.poll_ready_for_concurrent_call(func, cx).is_ready();
+                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..236bdf8d4c45 100644
--- a/crates/wasi-http/src/handler.rs
+++ b/crates/wasi-http/src/handler.rs
@@ -793,6 +793,12 @@ where
                     Some((pair, queue))
                 }
             ));
+            let func = match proxy {
+                #[cfg(feature = "p3")]
+                Proxy::P3(guest) => *guest.wasi_http_handler().func_handle().func(),
+                #[cfg(feature = "p2")]
+                Proxy::P2(guest) => *guest.wasi_http_incoming_handler().func_handle().func(),
+            };
             future::poll_fn(|cx| {
                 loop {
                     // First, and crucially first, poll `futures`. This way
@@ -839,6 +845,8 @@ where
                         Poll::Ready(None) | Poll::Pending => {}
                     }
 
+                    let is_ready = accessor.poll_ready_for_concurrent_call(func, cx).is_ready();
+
                     // 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(()));
                     }
 
diff --git a/crates/wasmtime/src/runtime/component/concurrent.rs b/crates/wasmtime/src/runtime/component/concurrent.rs
index c9f27f936a4e..f6b921b6717a 100644
--- a/crates/wasmtime/src/runtime/component/concurrent.rs
+++ b/crates/wasmtime/src/runtime/component/concurrent.rs
@@ -539,8 +539,8 @@ where
     /// otherwise returns `Poll::Pending`. If pending is returned then whenever
     /// the last remaining "interesting" task has exited the provided context's
     /// waker will be notified. Note that only the waker passed to the last call
-    /// to `poll_no_interesting_tasks` will be notified, so this is only
-    /// appropriate to use one-at-a-time.
+    /// to `poll_no_interesting_tasks` for the store will be notified, so this
+    /// is only appropriate to use once-at-a-time per store.
     ///
     /// The component model specification, as of this current date, does not
     /// have a distinction between "interesting" tasks and not. The current
@@ -579,6 +579,39 @@ where
             }
         })
     }
+
+    /// Poll to see if the component instance corresponding to the specified
+    /// 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).
+    ///
+    /// Returns `Poll::Ready(())` if the component instance is ready to run a
+    /// concurrent call, and otherwise returns `Poll::Pending`.  If pending is
+    /// returned then whenever the instance becomes ready for a call the
+    /// provided context's waker will be notified.  Note that only the waker
+    /// passed to the last call to `poll_ready_for_concurrent_call` for the
+    /// store will be notified (regardless of whether the same or different
+    /// `Func` is specified relative to earlier calls), so this is only
+    /// appropriate to use once-at-a-time per store.  Also note that the waker
+    /// may be notified when _any_ instance becomes callable (i.e. not
+    /// necessarily the last one polled), so this function must be called again
+    /// to determine if the instance of interest is ready.
+    pub fn poll_ready_for_concurrent_call(&self, func: Func, cx: &mut Context<'_>) -> Poll<()> {
+        self.with(|mut access| {
+            let store = access.as_context_mut().0;
+            let (_, _, _, raw_options) = func.abi_info(store);
+            let instance = func.instance().runtime_instance(raw_options.instance);
+            let state = store.instance_state(instance).concurrent_state();
+            if state.backpressure == 0 {
+                Poll::Ready(())
+            } else {
+                store
+                    .concurrent_state_mut_without_forcing_current_thread()
+                    .ready_for_concurrent_call_waker = Some(cx.waker().clone());
+                Poll::Pending
+            }
+        })
+    }
 }
 
 /// Represents a task which may be provided to `Accessor::spawn`,
@@ -1983,6 +2016,9 @@ impl StoreOpaque {
     /// Iterate over `InstanceState::pending`, moving any ready items into the
     /// "high priority" work item queue.
     ///
+    /// Also, notify `ConcurrentState::ready_for_concurrent_call_waker` if
+    /// present.
+    ///
     /// See `GuestCall::is_ready` for details.
     fn partition_pending(&mut self, instance: RuntimeInstance) -> Result<()> {
         for (thread, kind) in
@@ -2000,6 +2036,14 @@ impl StoreOpaque {
             }
         }
 
+        if let Some(waker) = self
+            .concurrent_state_mut()?
+            .ready_for_concurrent_call_waker
+            .take()
+        {
+            waker.wake();
+        }
+
         Ok(())
     }
 
@@ -5260,6 +5304,12 @@ pub struct ConcurrentState {
     ///
     /// Used in the implementation of `Accessor::poll_no_interesting_tasks`.
     interesting_tasks_empty_waker: Option<Waker>,
+
+    /// Single waker to notify when a component instance goes from
+    /// not-concurrently-callable to concurrently-callable.
+    ///
+    /// Used in the implementation of `Accessor::poll_ready_for_concurrent_call`.
+    ready_for_concurrent_call_waker: Option<Waker>,
 }
 
 impl Default for ConcurrentState {
@@ -5276,6 +5326,7 @@ impl Default for ConcurrentState {
             global_error_context_ref_counts: BTreeMap::new(),
             interesting_tasks: 0,
             interesting_tasks_empty_waker: None,
+            ready_for_concurrent_call_waker: None,
         }
     }
 }
@@ -5374,6 +5425,7 @@ impl ConcurrentState {
             global_error_context_ref_counts: _,
             interesting_tasks: _,
             interesting_tasks_empty_waker: _,
+            ready_for_concurrent_call_waker: _,
         } = self;
 
         for entry in table.get_mut().iter_mut() {